Chapter 24
Plant Constituents as Oviposition Deterrents to Lepidopterous Insects J. A. A. Renwick Boyce Thompson Institute, Tower Road, Ithaca, NY 14853
The natural resistance of plants to herbivorous insects can often be explained by the presence of specific metabolites that act as toxins or as behavior-modifying agents. Oviposition deterrents can offer a first line of defense against insect pests, and extracts of non-host plants have been effective in protecting otherwise susceptible hosts. A search for active plant constituents that cause avoidance of treated plants for egg laying has led to examination of unacceptable plant species which are closely related to preferred species. The cabbage butterfly, Pieris rapae lays eggs on most members of the Cruciferae, but a few species such as Erysimum cheiranthoides are avoided. Potent oviposition deterrents have been isolated from this plant and characterized as cardenolides. Any s e a r c h f o r n a t u r a l p r o d u c t s t h a t m i g h t b e u s e d t o c o n t r o l i n s e c t s i n e v i t a b l y leads us t o the n a t u r a l chemical defense systems t h a t p l a n t s have e v o l v e d through t h e ages t o p r o t e c t themselves. The n a t u r a l r e s i s t a n c e o f p l a n t s a g a i n s t invaders t a k e s many d i f f e r e n t f o r m s , b o t h p h y s i c a l a n d c h e m i c a l , a n d p o s s i b l e m e c h a n i s m s h a v e b e e n t h e s u b j e c t o f many r e v i e w s ( 1 , 2, !> 4, 5.) . T h i s d i s c u s s i o n w i l l b e c o n f i n e d t o t h e c h e m i c a l factors involved. A l l e l o c h e m i c a l s t h a t s e r v e t o p r o t e c t p l a n t s f r o m i n s e c t s may f u n c t i o n i n two ways: (1) b y a f f e c t i n g i n s e c t development and s u r v i v a l on t h e p l a n t , o r (2) b y i n f l u e n c i n g i n s e c t behavior. The b e h a v i o r a l e v e n t s o f most i n t e r e s t h e r e a r e t h o s e i n v o l v e d i n t h e process o f host s e l e c t i o n . Observations on the avoidance o f s p e c i f i c plants by insects can provide the f i r s t clues that p r o t e c t i v e c h e m i c a l s may b e p r e s e n t . More d e t a i l e d s t u d i e s o n host preferences can provide information on p o s i t i v e as w e l l as negative s t i m u l i a f f e c t i n g host f i n d i n g andacceptance. I f we k n o w w h a t c h e m i c a l s m e d i a t e t h i s b e h a v i o r , we m i g h t h a v e a b a s i s for genetic manipulation o f crop plants o r f o r using chemicals directly toprotect susceptible plants.
c
0097-6156/88/0380-0378$06.00/0 1988 American Chemical Society
24.
RENWICK
Plant Constituents as Oviposition Deterrents
Chemical Mediation
of Host
379
Selection
H o s t s e l e c t i o n b y i n s e c t s i n v o l v e s one o r m o r e b e h a v i o r a l r e s p o n s e s t h a t may b e m e d i a t e d b y p l a n t c o n s t i t u e n t s . These i n c l u d e o r i e n t a t i o n , o v i p o s i t i o n and f e e d i n g (6, 7 ) . However, these phases are not always c l e a r l y separated. For example, o v i p o s i t i o n g e n e r a l l y cannot occur w i t h o u t o r i e n t a t i o n to the t a r g e t p l a n t , so a n a l y s i s o f the f a c t o r s a f f e c t i n g o v i p o s i t i o n o f t e n r e q u i r e s c o n s i d e r a t i o n of the s t i m u l i t h a t e l i c i t l a n d i n g . The c h e m i c a l f a c t o r s m e d i a t i n g l a n d i n g o n a n d a c c e p t a n c e o f potential host plants for oviposition include attractants, r e p e l l e n t s , s t i m u l a n t s and d e t e r r e n t s . The i m p o r t a n c e o f u n d e r s t a n d i n g t h e i n t e r p l a y among t h e s e f a c t o r s h a s b e e n r e c o g n i z e d a n d e m p h a s i z e d b y many a u t h o r s (7., 8) · B u t t h e i d e a o f u t i l i z i n g the behavior-modifying chemicals that a f f e c t o v i p o s i t i o n t o combat i n s e c t p e s t s has n o t been w i d e l y i n v e s t i g a t e d . The concept of i n t e r f e r i n g with o v i p o s i t i o n i s p a r t i c u l a r l y appealing, s i n c e i t c o u l d provide the o p p o r t u n i t y to b l o c k i n s e c t i n f e s t a t i o n s b e f o r e a n y damage c a n occur. Manipulation
of
Oviposition
S e v e r a l d i f f e r e n t s t r a t e g i e s m i g h t be e m p l o y e d t o m a n i p u l a t e o v i p o s i t i o n by i n s e c t p e s t s . F i r s t l y , we m i g h t i n t e r f e r e w i t h o r i e n t a t i o n or l a n d i n g by i n t e r c r o p p i n g w i t h o d o r i f e r o u s p l a n t s or t h r o u g h the d i r e c t use o f r e p e l l e n t s . Secondly, o v i p o s i t i o n d e t e r r e n t s m i g h t be i n t r o d u c e d i n t o c r o p p l a n t s as a r e s u l t o f p l a n t b r e e d i n g o r r e c o m b i n a n t DNA t e c h n i q u e s , o r d e t e r r e n t s could be s p r a y e d d i r e c t l y on t h e p l a n t s t o be p r o t e c t e d . Thirdly, o v i p o s i t i o n s t i m u l a n t s m i g h t be u s e d t o " f o o l " t h e i n s e c t s i n t o l a y i n g t h e i r eggs on n o n - h o s t p l a n t s w h i c h w o u l d be u n s u i t a b l e f o r l a r v a l development. G e n e t i c m a n i p u l a t i o n m i g h t a l s o be p o s s i b l e , i n t h i s c a s e , t o remove s t i m u l a n t f r o m the c r o p p l a n t s . The c o n c e p t o f i n t e r f e r i n g w i t h o v i p o s i t i o n a s a means o f i n s e c t c o n t r o l has y e t t o be s e r i o u s l y t e s t e d i n t h e f i e l d . Several q u e s t i o n s n e e d t o be a n s w e r e d b e f o r e t h e s u g g e s t e d s t r a t e g i e s c a n be i m p l e m e n t e d . The u s e o f d e t e r r e n t s may l e a d t o h a b i t u a t i o n o f the t a r g e t i n s e c t s . T h e r e f o r e , t h e s u c c e s s o f t h i s a p p r o a c h may depend on t h e p r e s e n c e o f a l t e r n a t e s i t e s f o r o v i p o s i t i o n . I t i s l i k e l y that combinations of possible s t r a t e g i e s w i l l provide the b e s t r e s u l t s , and the i d e a o f u s i n g t r a p c r o p s , o r p l a n t s t r e a t e d with stimulants, along with deterrent-treatment of the main crop, has c o n s i d e r a b l e merit. D e s p i t e t h e w i d e s p r e a d i n t e r e s t i n o v i p o s i t i o n as a t a r g e t s t a g e f o r i n s e c t c o n t r o l and r a p i d l y e x p a n d i n g r e s e a r c h programs i n t h e f i e l d , r e l a t i v e l y few o f t h e c h e m i c a l s i n v o l v e d h a v e a c t u a l l y been i d e n t i f i e d . Probably the b e s t p r o g r e s s i n the area has b e e n i n t h e i s o l a t i o n and i d e n t i f i c a t i o n o f v o l a t i l e compounds t h a t a t t r a c t o r s t i m u l a t e s p e c i a l i s t f l i e s s u c h as t h e o n i o n f l y and t h e c a r r o t f l y ( 9 , 10, 11, 1 2 ) . These compounds f u n c t i o n as a t t r a c t a n t s a n d / o r a r r e s t a n t s so t h a t o v i p o s i t i o n i s t h e end result. But the p o s s i b l e i n v o l v e m e n t o f c o n t a c t s t i m u l i t h a t t r i g g e r t h e f i n a l a c t o f egg d e p o s i t i o n c a n n o t be e x c l u d e d . Among the s p e c i a l i s t b u t t e r f l i e s , the l a r g e w h i t e cabbage b u t t e r f l y ,
380
BIOLOGICALLY ACTIVE NATURAL PRODUCTS
P i e r i s b r a s s i c a e . has been w i d e l y s t u d i e d i n Europe. This b u t t e r f l y i s s t i m u l a t e d t o o v i p o s i t by g l u c o s i n o l a t e s p r e s e n t i t s c r u c i f e r host plants (13). Another group o f b u t t e r f l i e s p r e s e n t l y b e i n g e x t e n s i v e l y s t u d i e d are the s w a l l o w t a i l s . F l a v a n o n e g l y c o s i d e s t h a t s t i m u l a t e o v i p o s i t i o n by P a p i l i o p r o t e n o r have been i d e n t i f i e d i n Japan (14),
in
and Feeny and c o w o r k e r s r e c e n t l y i d e n t i f i e d a c i d i c f l a v o n o i d s t h a t a c t s y n e r g i s t i c a l l y w i t h a n o t h e r p l a n t component t o s t i m u l a t e o v i p o s i t i o n by the u m b e l l i f e r - f e e d i n g P a p i l i o polyxenes (15). In a l l the b u t t e r f l i e s s t u d i e d , the c r i t i c a l s t i m u l i are perceived t h r o u g h t a r s a l r e c e p t o r s (13., 1 5 , 16) , s o c o n t a c t w i t h t h e p l a n t i s necessary for host recognition. The f a c t o r s a f f e c t i n g o v i p o s i t i o n by moths a r e s i m i l a r t o t h o s e f o r b u t t e r f l i e s , and the s u b j e c t h a s b e e n r e v i e w e d b y Ramaswamy ( 1 7 ) . Oviposition Deterring
Pheromones
The r o l e o f i n h i b i t o r y c o m p o u n d s t h a t d i s c o u r a g e o v i p o s i t i o n o n u n s u i t a b l e p l a n t s has l o n g been r e c o g n i z e d , b u t has o n l y r e c e n t l y b e e n e m p h a s i z e d by Jermy and S z e n t e s i ( 1 8 ) . A l t h o u g h we n e e d t o know as much as p o s s i b l e a b o u t p o s i t i v e as w e l l as n e g a t i v e inputs i n p l a n t - i n s e c t r e l a t i o n s h i p s , from a p r a c t i c a l p o i n t of view, the i d e a o f b l o c k i n g o v i p o s i t i o n appears to o f f e r the most promise. The p o t e n t i a l o f o v i p o s i t i o n d e t e r r e n t s h a s r e c e n t l y b e e n h i g h l i g h t e d by the d i s c o v e r y o f o v i p o s i t i o n d e t e r r i n g pheromones. P i o n e e r i n g w o r k b y P r o k o p y ( 1 9 ) h a s s h o w n t h a t many s p e c i e s o f f r u i t f l i e s r e l e a s e a m a r k i n g c h e m i c a l d u r i n g and a f t e r oviposition. T h i s c h e m i c a l i s smeared onto the f r u i t s u r f a c e and s e r v e s t o d i s c o u r a g e f u r t h e r o v i p o s i t i o n by o t h e r f e m a l e f l i e s on that f r u i t . I n t h i s way, o v e r c r o w d i n g i s a v o i d e d and the l a r v a e c a n d e v e l o p w i t h l i t t l e o r no c o m p e t i t i o n . Similar oviposition
24.
RENWICK
381
Plant Constituents as Oviposition Deterrents
d e t e r r i n g pheromones ( e p i d e i c t i c pheromones) have b e e n f o u n d i n a v a r i e t y o f i n s e c t s where r e s o u r c e s a r e l i m i t e d and a d e q u a t e spacing of larvae i s e s s e n t i a l (20). I n most o f t h e s e c a s e s , p h y s i c a l as w e l l as c h e m i c a l c u e s p l a y a r o l e i n t h e spacing mechanism. For example, cowpea w e e v i l s a c h i e v e a l m o s t p e r f e c t d i s t r i b u t i o n o f t h e i r eggs on a v a i l a b l e s e e d s by a c o m b i n a t i o n o f p h y s i c a l r e c o g n i t i o n and c h e m i c a l m a r k i n g o f eggs ( 2 1 ) . The cabbage b u t t e r f l y , P i e r i s b r a s s i c a e . a l s o u s e s unknown c h e m i c a l s as w e l l as v i s u a l c u e s t o r e c o g n i z e t h e p r e s e n c e o f egg b a t c h e s on h o s t p l a n t s (22., 23.) . The i d e n t i f i c a t i o n o f o v i p o s i t i o n d e t e r r i n g pheromones has p r o v e d t o be e x t r e m e l y d i f f i c u l t , b u t t h e f i r s t s u c c e s s has r e c e n t l y been r e p o r t e d by a group i n S w i t z e r l a n d . E l e c t r o p h y s i o l o g i c a l m o n i t o r i n g was u s e d t o i s o l a t e t h e p h e r o m o n e o f t h e E u r o p e a n c h e r r y f r u i t f l y and t h e a c t i v e compound has b e e n c h a r a c t e r i z e d (24).
OH F i e l d t e s t s o f e x t r a c t s o f t h i s pheromone had p r e v i o u s l y t h a t p r a c t i c a l a p p l i c a t i o n i s a r e a l p o s s i b i l i t y (2j>) . Plant
Constituents
Deterring
shown
Oviposition
The s u c c e s s o f s t u d i e s o n o v i p o s i t i o n d e t e r r i n g p h e r o m o n e s h a s h e l p e d i n b o o s t i n g r e s e a r c h on p l a n t - p r o d u c e d d e t e r r e n t s . Several c a s e s h a v e now b e e n r e p o r t e d w h e r e i n s e c t i n j u r y r e s u l t s i n t h e r e l e a s e o f p l a n t c o n s t i t u e n t s t h a t may f u n c t i o n a s o v i p o s i t i o n deterrents. One e x a m p l e i s t h e o l i v e f r u i t f l y , w h i c h p u n c t u r e s the f r u i t as i t l a y s i t s eggs, and the j u i c e s f l o w i n g f r o m the wound c o n t a i n c h e m i c a l s t h a t d e t e r f u r t h e r o v i p o s i t i o n ( 2 6 ) . A n o t h e r s p a c i n g m e c h a n i s m was f o u n d f o r t h e c a b b a g e l o o p e r , T r i c h o p l u s i a n i . T h i s moth l a y s i t s eggs e v e n l y o v e r a v a i l a b l e p l a n t s and a v o i d s p l a n t s t h a t a r e a l r e a d y o c c u p i e d by feeding larvae. The l a r v a l f r a s s was f o u n d t o b e a s o u r c e o f o v i p o s i t i o n d e t e r r e n t (27.), b u t f u r t h e r s t u d i e s s h o w e d t h a t d i s r u p t i o n o f p l a n t t i s s u e by the f e e d i n g l a r v a e c o u l d account f o r r e l e a s e o f a c t i v e compounds f r o m t h e p l a n t ( 2 8 ) . O v i p o s i t i o n d e t e r r e n t s have now b e e n f o u n d i n f r a s s o f s e v e r a l i n s e c t s i n c l u d i n g t h e E u r o p e a n c o r n b o r e r a n d s p e c i e s o f S p o d o p t e r a ( 2 9 , 30, 3 1 ) , a n d p l a n t c o n s t i t u e n t s may b e r e s p o n s i b l e f o r t h e a c t i v i t y i n m o s t o f t h e s e cases. I t i s now c l e a r t h a t s e v e r a l s o u r c e s o f n a t u r a l o v i p o s i t i o n d e t e r r e n t s are a v a i l a b l e to us. The m a r k i n g p h e r o m o n e s r e p r e s e n t a group o f p o t e n t s p e c i e s - s p e c i f i c agents f o r i n s e c t s w h i c h depend on a d e q u a t e s p a c i n g f o r t h e i r s u r v i v a l . Plant constituents offer a more g e n e r a l s o u r c e o f b i o l o g i c a l l y a c t i v e c h e m i c a l s . T h e s e may be r e l e a s e d f r o m damaged h o s t p l a n t s , and t h u s p l a y a r o l e i n t h e d i s t r i b u t i o n o f i n s e c t p o p u l a t i o n s , o r compounds f r o m n o n - h o s t
382
BIOLOGICALLY ACTIVE NATURAL PRODUCTS
p l a n t s m i g h t be more g e n e r a l l y i n v o l v e d i n p r o t e c t i o n f r o m a v a r i e t y of herbivores. B o t h v o l a t i l e and n o n - v o l a t i l e n e g a t i v e s i g n a l s may b e p r o v i d e d b y a p l a n t . The u s e o f v o l a t i l e r e p e l l e n t s t o p r o t e c t a c r o p p l a n t has o f t e n b e e n s u g g e s t e d , and i n t e r c r o p p i n g w i t h h e r b s or o t h e r f r a g r a n t p l a n t s i s an a t t e m p t to c a p i t a l i z e o n t h i s p r i n c i p l e ( 3 2 , 3,3, 3 4 ) . However, most e f f o r t s t o use o v i p o s i t i o n d e t e r r e n t s as p r o t e c t i v e a g e n t s i n v o l v e nonv o l a t i l e p l a n t c o n s t i t u e n t s , w h i c h a r e l i k e l y t o h a v e a more persistent effect. Some e a r l y w o r k b a s e d o n i d e a s o f o r g a n i c g a r d e n e r s i n c l u d e d the use o f tomato homogenates a g a i n s t cabbage b u t t e r f l i e s and c h e s t n u t e x t r a c t s a g a i n s t s u g a r b e e t moths (35. 36). These s t u d i e s have been f o l l o w e d by s e v e r a l o t h e r s aimed a t lepidopterous pests of various crop p l a n t s (Table I). The usual a p p r o a c h , t h e r e f o r e , has b e e n t o t e s t e x t r a c t s o f u n r e l a t e d , nonh o s t p l a n t s as d e t e r r e n t s a g a i n s t a p a r t i c u l a r i n s e c t . Oviposition Deterrents
f o r Pieris
rapae
I n i t i a l s t u d i e s on the cabbage b u t t e r f l y , P i e r i s r a p a e . i n c l u d e d a s u r v e y o f d e t e r r e n t a c t i v i t y i n a v a r i e t y o f h o s t and n o n - h o s t plants. I n c h o i c e b i o a s s a y s w i t h t r e a t e d and u n t r e a t e d cabbage p l a n t s i n greenhouse cages, hexane e x t r a c t s of non-host p l a n t s were a l l d e t e r r e n t (44). However, hexane e x t r a c t s o f h o s t p l a n t s were a l s o d e t e r r e n t . T h e s e r e s u l t s s u g g e s t e d t h a t many n o n s p e c i f i c c h e m i c a l s i n d a m a g e d t i s s u e s o f p l a n t s may a c t as deterrents. B u t w h e n w a t e r s o l u b l e m a t e r i a l f r o m t h e same p l a n t s was t e s t e d , c l e a r d i f f e r e n c e s b e t w e e n h o s t s a n d n o n - h o s t s w e r e seen (44). The l a c k o f d e t e r r e n t a c t i v i t y i n w a t e r e x t r a c t s o f h o s t p l a n t s was n o t s u r p r i s i n g s i n c e t h e s e e x t r a c t s a r e k n o w n t o c o n t a i n o v i p o s i t i o n stimulants (45). As a r e s u l t o f t h e s e s t u d i e s , a t t e n t i o n h a s b e e n f o c u s e d o n c r u c i f e r s , w h i c h we m i g h t e x p e c t t o be a t t r a c t i v e t o c a b b a g e b u t t e r f l i e s , b u t w h i c h a r e rejected after landing. Two e x a m p l e s o f u n a c c e p t a b l e c r u c i f e r s , Erysimum c h e i r a n t h o i d e s and C a p s e l l a b u r s a - p a s t o r i s . clearly c o n t a i n p o w e r f u l d e t e r r e n t s (44)· I f these p l a n t s a l s o produce s t i m u l a n t s , t h e d e t e r r e n t s must be p a r t i c u l a r l y p o t e n t t o o u t w e i g h the p o s i t i v e e f f e c t s of the s t i m u l a n t . T h i s argument has provided the r a t i o n a l e f o r our approach o f s t u d y i n g p l a n t s t h a t are a v o i d e d by an i n s e c t b u t w h i c h are c l o s e l y r e l a t e d t o p r e f e r r e d h o s t s . Erysimum c h e i r a n t h o i d e s i s a s m a l l i n c o n s p i c u o u s p l a n t w i t h l i t t l e f o l i a g e for chemical studies. But p r o p a g a t i o n i n the g r e e n h o u s e i s e a s y , and k i l o g r a m q u a n t i t i e s were p r o d u c e d o v e r a p e r i o d o f a few months. S e p a r a t i o n o f p o l a r e x t r a c t s by p a r t i t i o n i n g b e t w e e n w a t e r a n d b u t a n o l p r o v i d e d a c o n v e n i e n t means o f s h o w i n g t h a t b o t h s t i m u l a n t and d e t e r r e n t a r e p r e s e n t i n t h i s p l a n t (46). When b u t a n o l e x t r a c t s o f E. c h e i r a n t h o i d e s w e r e s u b j e c t e d t o r e v e r s e d p h a s e HPLC, w i t h a w a t e r - a c e t o n i t r i l e g r a d i e n t , a l l t h e d e t e r r e n t a c t i v i t y was o b t a i n e d i n a f r a c t i o n e l u t i n g w i t h a b o u t 28% a c e t o n i t r i l e . Maximum UV a b s o r p t i o n a t 219 nm f o r t h e m a j o r p e a k s s u g g e s t e d t h a t t h e s e c o m p o u n d s may b e c a r d e n o l i d e s . A p o s i t i v e r e a c t i o n w i t h Keddes' Reagent c o n f i r m e d the cardenolide c h a r a c t e r o f t h e a c t i v e c o m p o n e n t s ( 4 7 ) a n d two o f t h e g l y c o s i d e s have been p o s i t i v e l y i d e n t i f i e d (48).
Table I .
P l a n t e x t r a c t s t e s t e d as o v i p o s i t i o n d e t e r r e n t s lepidopterous pests
Insect
Plant
Pieris
383
Plant Constituents as Oviposition Deterrents
24. RENWICK
Extract
against
Reference
brassicae
P.
rapae
Ρ.
napi
Lundgren
Scrobipalpa ocellatella
Castanea s a t i v a (chestnut)
Heliothis virescens
(35)
Robert & Blaisinger (36)
Tingle & Mitchell
(37)
Sambucus s i m p s o n i i (elderberry)
Tingle & Mitchell
(38)
Spodoptera exigua S. e r i d a n i a
Amaranthus h y d r i d u s (pigweed)
Mitchell & Heath (39)
Spodoptera
corn
Williams e t a l . (30)
H.
virescens
Plutella
Cydia
frugiperda
xvlostella
pomonella
leaves
various
herbs
various medicinal
plants
Dover
(40)
Adivardi & Benz (41)
Spodoptera
litura
Neem k e r n e l
Joshi & Sitaramaiah (42)
Spodoptera
frugiperda
Neem k e r n e l
Hellpap & Mercado (43)
384
BIOLOGICALLY ACTIVE NATURAL PRODUCTS
The big question that now remains is whether these cardenolides could be effective in protecting cabbage plants in the field. The results of preliminary field tests of crude extracts suggest that some degree of control is possible (49). The concentrations of cardenolides required are likely to be in the microgram per plant range, well below mammalian toxicity levels. However, the toxic reputation of cardenolides may make acceptance of these compounds in an agricultural system difficult, and research efforts are now being focused on other crucifer plants. The approach of isolating deterrents from unacceptable plants that are related to hosts appears to be promising, and this work should serve as a model system for future studies. Acknowledgments Research was supported in part by the U.S. Department of Agriculture under Agreement No. 86-CRCR-1-2007. Literature Cited 1. Painter, R.H. "Insect Resistance in Crop Plants"; University Press of Kansas: Lawrence/London, 1951; 520 pp. 2. Panda, N. "Principles of Host-plant Resistance to Insect Pests"; Allanheld/Universe; New York, 1979; 386 pp. 3. Hedin, P.A., ed. "Plant Resistance to Insects"; Am. Chem. Soc. Symp. Ser. 1983, 208, 375 pp. 4. Green, M.B. & P.A. Hedin, eds. "Natural Resistance of Plants to Pests; Am. Chem. Soc. Svmp. Ser. 1986, 296, 243 pp. 5. Robert, P.C. Agronomie 1986, 6, 127-42. 6. Renwick, J.A.A. In: "Plant Resistance to Insects" (P.A. Hedin, ed.); Am. Chem. Soc. Symp. Ser. 1983, 208, 199-213. 7. Miller, J.R.; Strickler, K.L. In: "Chemical Ecology of Insects" (W.J. Bell & R.T. Cardé, eds.); Chapman and Hall: London, 1984; 127-57. 8. Dethier, V.G. Ent. exp. appl. 1982, 31, 49-56. 9. Matsumoto, Y.; Thorsteinson, A.J. Applied Entomol. and Zool. 1968, 3, 5-12. 10. Ishikawa, Y.; Ikeshoji, T.; Matsumoto, Y. Applied Entomol. and Zool. 1978, 13, 115-22. 11. Vernon, R.S.; Pierce, H.D., Jr.; Borden, J.H.; Oehlschlager, A.C. Environ. Entomol. 1978, 7, 728-31. 12. Guerin, P.M., Städler, Ε.; Buser, H.R. J. Chem. Ecol. 1983, 9, 843-61. 13. Ma, W.C.; Schoonhoven, L.M. Ent. exp. appl. 1973, 16, 343-57. 14. Honda, K. J. Chem. Ecol. 1986, 12, 1999-2010. 15. Feeny, P.P. 1987, personal communication. 16. Traynier, R.M.M. Physiol. Entomol. 1979, 4, 87-96. 17. Ramaswamy, S.B. J. Insect Physiol. (in press). 18. Jermy, T.; Szentesi, ÁEnt. exp. appl. 1978; 24, 258-71. 19. Prokopy, R.J. Environ. Entomol. 1972, 1, 326-32. 20. Prokopy, R.J. In: "Semiochemicals. Their Role in Pest Control" (D.A. Nordlund, R.L. Jones, W.J. Lewis, eds.); WileyInterscience: New York, 1981; pp 181-213. 21. Messina, F.J.; Renwick, J.A.A. Ent. exp. appl. 1985, 37, 2415. 22. Rothschild, M.; Schoonhoven, L.M. Nature 1977, 266, 352-5.
24. RENWICK
Plant Constituents as Oviposition Deterrents
385
23. Behan, M.; Schoonhoven, L.M. Ent. exp. appl. 1978, 24, 163-79. 24. Hurter, J.; Boller, E.F.; Städler, Ε.; Buser, H.R.; Bosshard, N.U.; Damm, L.; Kozlowski, M.W.; Schöni, R.; Raschdorf, F.; Dahinden, R.; Schlumpf, E.; Fritz, H.; Richter, W.J.; Schreiber, J. Experientia 1987, 43, 157-64. 25. Katsoyannos, B.I.; Boiler, E.F. Environ. Entomol. 1976, 5, 151-2. 26. Cirio, U. Redia 1971, 52, 577-600. 27. Renwick, J.A.A.; Radke, C.D. Environ. Entomol. 1980, 9, 31820. 28. Renwick, J.A.A.; Radke, C.D. Ent. exp. appl. 1981, 30, 201-4. 29. Dittrick, L.E.; Jones, R.L.; Chiang, H.C. J. Insect Physiol. 1983, 29, 119-21. 30. Williams, A.L.; Mitchell, E.R.; Heath, R.R.; Barfield, C.S. Environ. Entomol. 1986, 15, 327-30. 31. Hilker, M. Naturwissenschaften 1985, 72, 485-6. 32. Perrin, R.M.; Phillips, M.L. Ent. exp. appl. 1978, 24 385-93. 33. Tahvanainen, J.O.; Root, R.B. Oecologia 1972, 321-46. 34. Saxena, K.N.; Basit, A. J. Chem. Ecol. 1982, 8, 329-38. 35. Lundgren, L. Zoologica Scripta 1975, 4, 253-8. 36. Robert, P.C.; Blaisinger, P. Ent. exp. appl. 1978, 24, 632-6. 37. Tingle, F.C.; Mitchell, E.R. J. Chem. Ecol. 1984, 10, 101-13. 38. Tingle, F.C.; Mitchell, E.R. J. Chem. Ecol. 1986, 12, 152331. 39. Mitchell, E.R.; Heath, R.R. J. Chem. Ecol. 1985, 11, 609-17. 40. Dover, J.W. Ent. exp. appl. 1985, 39, 177-82. 41. Abivardi, C.; Benz, G. Mitt. Schweiz. Entomol. Gesell 1986, 59, 31-8. 42. Joshi, B.G.; Sitaramaiah, S. Phytoparasitica 1979, 7, 199-202. 43. Hellpap, C.; Mercado, J . C . J. Appl. Ent. 1986, 102, 463-7. 44. Renwick, J.A.A.; Radke, C.D. Ent. exp. appl. 1985, 39, 21-6. 45. Renwick, J.A.A.; Radke, C.D. Environ. Entomol. 1983, 12, 44650. 46. Renwick, J.A.A.; Radke, C.D. J. Chem. Ecol. 1987, 13, 1771-6. 47. Renwick, J.A.A.; Radke, C.D.; Sachdev, K. in preparation. 48. Sachdev, K.; Renwick, J.A.A. in preparation. 49. Dimock, M.B.; Renwick, J.A.A. in preparation. RECEIVED April
1, 1988
