Light-Activated Pesticides - American Chemical Society

Chapter 14

Charge of the Light Brigade: Phototoxicityasa Defense Against Insects M. R. Berenbaum Department of Entomology, University of Illinois, Urbana, IL 61801-3795

Sunlight i s used by many plants to activate secondary compounds and to enhance their t o x i c i t y . This a c t i v a t i o n can occur i n at least two ways. Photons can be absorbed by plant chemicals, such as the furanocoumarins t y p i c a l of the Umbelliferae and Rutaceae, to a l t e r the electron configuration and form a highly reactive excited state; the excited state molecule can then interact d i r e c t l y with biomolecules such as DNA, proteins or membrane l i p i d s with concomitant toxic effects. A l t e r n a t i v e l y , as i s the case for polyacetylenes t y p i c a l of the Compositae and quinones of the Guttiferae, photopromoted excited states can interact with oxygen to form the reactive molecule s i n g l e t oxygen, which then can i n t e r f e r e chemically with other biomolecules. Toxicity enhancement by sunlight i s increased still further by v i r t u e of the fact that certain wavelengths can stimulate enhanced biosynthesis and increased accumulation of phototoxins. N a t u r a l l y occurring phototoxins occur i n a diverse array of plant f a m i l i e s and represent a v a r i e t y of b i o s y n t h e t i c a l l y unrelated structures. Many of these chemicals are toxic to generalized feeders , p a r t i c u l a r l y i n the presence of l i g h t of the appropriate wavelengths. E s s e n t i a l l y every phototoxic plant i s associated with oligophagous species which have overcome the defensive chemistry of their hosts. Mechanisms of resistance include behavioral resistance i n the form of l e a f - r o l l i n g , web-spinning, and other forms of concealed feeding which s h i e l d the insect from damaging wavelengths, physical resistance i n the form of body pigments that s e l e c t i v e l y absorb damaging wavelengths or quench excited states, or biochemical resistance i n the form of enzymatic degradation of phototoxic molecules. Sunlight, then, i s an important e c o l o g i c a l factor mediating the evolutionary responses between plants and herbivorous insects.

0097-6156/87/0339-0206$06.00/0 © 1987 American Chemical Society

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Phototoxicity as a Defense Against Insects

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The concept of u s i n g l i g h t energy f o r d e f e n s i v e purposes, ( v i z , the " S t r a t e g i c Defense I n i t i a t i v e " of the Reagan a d m i n i s t r a t i o n ) i s h a r d l y an i n n o v a t i o n ; p l a n t s have i n c o r p o r a t e d s u n l i g h t i n t o t h e i r d e f e n s i v e armamentarium f o r m i l l e n i a (1). Many p l a n t a l l e l o c h e m i c a l s can absorb photons of l i g h t energy at p a r t i c u l a r w a v e l e n g t h s . T h i s energy can t r a n s f o r m a m o l e c u l e from i t s l o w e s t e l e c t r o n energy s t a t e or ground s t a t e to a h i g h e r or e x c i t e d s t a t e . These e x c i t e d s t a t e s are h i g h l y r e a c t i v e and p h o t o t o x i c p l a n t c h e m i c a l s can r e a c t w i t h a v a r i e t y of b i o m o l e c u l e s . In the case of f u r a n o c o u m a r i n s , f o r example, compounds t y p i c a l l y found In p l a n t s i n the f a m i l i e s Rutaceae and Umbel 1 i f e r a e , e x c i t e d t r i p l e t s r e a c t w i t h p y r i m i d i n e bases i n DNA to form c y c l o a d d u c t s t h a t i m p a i r t r a n s c r i p t i o n and r e p l i c a t i o n . In many o t h e r p h o t o s e n s i t i z e r s , the e x c i t e d t r i p l e t s t a t e r e a c t w i t h m o l e c u l a r oxygen, which i n i t s ground s t a t e i s a t r i p l e t . The s i n g l e t oxygen t h a t r e s u l t s i s h i g h l y r e a c t i v e and can damage p r o t e i n s , l i p i d s and DNA. Ground s t a t e oxygen can a l s o form s u p e r o x i d e r a d i c a l s i n the presence of a p h o t o s e n s i t i z e r ; these m o l e c u l e s can damage l i p i d s , DNA, and p o l y s a c c h a r i d e s (1). S i n c e the t a r g e t s i t e s f o r p h o t o s e n s i t i z i n g compounds are o f t e n important b i o m o l e c u l e s , n a t u r a l p h o t o s e n s i t i z e r s are b r o a d l y b i o c i d a l . However, i t has l o n g been r e c o g n i z e d (2) t h a t h e r b i v o r o u s i n s e c t s , as a major s e l e c t i v e f o r c e on p l a n t s , are l i k e l y to be a p r i n c i p a l m o t i v e f o r c e behind the e v o l u t i o n a r y p r o l i f e r a t i o n of t o x i c c h e m i c a l s In p l a n t t i s s u e . Such i s l i k e l y the case f o r p h o t o s e n s i t i z e r s as w e l l . N a t u r a l p h o t o t o x i n s were f i r s t shown to have i n s e c t i c i d a l p r o p e r t i e s i n 1978 (3); s i n c e t h a t time, a t l e a s t n i n e b i o s y n t h e t i c a l l y d i s t i n c t c l a s s e s of p h o t o t o x i c i n s e c t i c i d e s have been i d e n t i f i e d ( T a b l e I ) . S u n l i g h t , then, can a c t at the c h e m i c a l l e v e l , enhancing the t o x i c i t y of d e f e n s i v e c h e m i c a l s s y n t h e s i z e d by p l a n t s . S u n l i g h t can a l s o a f f e c t m e t a b o l i c r a t e s i n p l a n t s ; i n c r e a s i n g UV l i g h t i n t e n s i t y s e l e c t i v e l y s t i m u l a t e s enzyme a c t i v i t y and enhances b i o s y n t h e t i c r a t e s f o r a v a r i e t y o f n a t u r a l p r o d u c t s ( T a b l e I I ) . I n d u c t i o n of p h e n y l a l a n i n e ammonia l y a s e by u l t r a v i o l e t i r r a d i a t i o n , e.g., d i r e c t l y a f f e c t s p r o d u c t i o n of p h e n y l p r o p a n o i d s , coumarins, f l a v o n o i d s , acetophenones and l i g n a n s (Berenbaum 1987, i n p r e s s ) . M o r e o v e r , s u n l i g h t can a c t as an i n d i r e c t f a c t o r i n f l u e n c i n g the c h e m i c a l p r o f i l e of a p l a n t s p e c i e s . In t h a t w a v e l e n g t h and i n t e n s i t y are two f a c t o r s i n f l u e n c i n g p h o t o s y n t h e t i c r a t e s of p l a n t s , they can a l s o i n f l u e n c e a l l e l o c h e m i c a l p r o d u c t i o n i n those i n s t a n c e s i n w h i c h b i o s y n t h e s i s i s e n e r g y - l i m i t e d . Enhanced p h o t o s y n t h e t i c r a t e s p r o v i d e more energy to c h a n n e l i n t o b i o s y n t h e s i s (4).

LIGHT-ACTIVATED PESTICIDES

208

Table I . P l a n t d e r i v e d - p h o t o t o x i n s w i t h i n s e c t i c i d a l Class Acetylenes Benzopyrans and f u r a n s Benzylisoquinoline alkaloids Beta-carboline alkaloids Extended quinones Furanocoumarins

Furanochromones Furoquinoline alkaloids Thiophenes

Table I I .

properties

Reference 5, 6, 7

Source Compositae

A r e g u l l i n , t h i s volume Compositae B e r b e r i d a c e a e , Rutaceae, 8 Rubiaceae Rutaceae, Simaroubaceae 9, E. H e i n i n g e r , i n prep. G u t t i f e r a e , Polygonaceae 10 Leguminosae, 3, 11, 12, 1 3 , 14 Moraceae, Rutaceae, U m b e l l i f e r a e , Composite Solanaceae Rutaceae, U m b e l l i f erae 11, 15 Rutaceae 9, E. H e i n i n g e r , i n prep. Compositae 5, 7, 16, 17

P l a n t compounds induced o r i n c r e a s e d by l i g h t

Plant compound

L i g h t source

P l a n t source

Ref

Alkaloids Alkaloids Anthocyanins Betacyanins Cannabinoids Cardenolides Carotenoids DIMBOA Flavonoids Furanocoumarins

red and IR Visible Visible red UV Visible blue l i g h t Visible UV UV

tobacco lupines,tobacco many p l a n t s Centrospermae marijuana D i g i t a l i s lanata many s p e c i e s Zea mays Umbelliferae parsnip

Isoflavonoids Tannins Terpenes

UV "sunlight" "sunlight"

soybean oak Hymenaea courbaril

18 18 19 19 20 21 22 23 24 Berenbaum and Z a n g e r l 1987, i n press 25 26 27

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209

E f f i c a c y o f p h o t o t o x i c i t y as a defense a g a i n s t i n s e c t s No defense system i s u n b r e a c h a b l e , and l i g h t - d e p e n d e n t defense systems o f p l a n t s a r e no e x c e p t i o n . C o n t i n u i n g s e l e c t i o n by p l a n t c h e m i c a l s promotes the a c q u i s i t i o n o f r e s i s t a n c e by h e r b i v o r o u s i n s e c t s o v e r e v o l u t i o n a r y time. However, s e l e c t i o n by p h o t o t o x i n s d i f f e r s from the s t a n d a r d s c e n a r i o (e.g., 28) i n t h a t the s e l e c t i v e f o r c e promoting the e v o l u t i o n o f r e s i s t a n c e can e i t h e r be the c h e m i c a l i t s e l f o r the s u n l i g h t c o n f e r r i n g t o x i c i t y to the c h e m i c a l . Insect associates of phototoxic p l a n t s d i s p l a y a v a r i e t y of a d a p t a t i o n s t o p h o t o t o x i c p l a n t s t h a t e i t h e r reduce the c h e m i c a l r e a c t i v i t y o r p h y s i o l o g i c a l e f f e c t s o f the substances i n v o l v e d o r m i n i m i z e t h e i r exposure t o l e t h a l amounts o r w a v e l e n g t h s o f sunlight. Behavioral resistance B e h a v i o r a l r e s i s t a n c e t o a p h o t o t o x i n r e s u l t s e i t h e r from the f a i l u r e o f an i n s e c t to i n g e s t o r c o n t a c t a l e t h a l dose o f t o x i c a n t o r from the a b i l i t y o f an i n s e c t t o feed i n such a manner as t o reduce the amount o f l i g h t exposure b e l o w t h a t r e q u i r e d to a c t i v a t e a p h o t o t o x i n . Feeding i n a c o n c e a l e d manner i s c h a r a c t e r i s t i c o f a number o f i n s e c t a s s o c i a t e s o f a number o f p h o t o t o x i c p l a n t s . Modes of concealed feeding i n c l u d e l e a f mining, l e a f t y i n g , l e a f r o l l i n g , stem b o r i n g , s u b t e r r a n e a n r o o t f e e d i n g , o r b o r i n g i n t o buds o r f r u i t s . I n a l l these c a s e s , p l a n t t i s s u e s can e f f e c t i v e l y b l o c k s i g n i f i c a n t amounts o f damaging s u n l i g h t . For example, i n a s u r v e y of l e a f e p i d e r m a l t r a n s m i t t a n c e o f UV r a d i a t i o n i n 25 s p e c i e s o f p l a n t s , t r a n s m i t t a n c e i n most cases was l e s s than 10% and i n o v e r h a l f the s p e c i e s ranged from 1 to 5% (29). B e h a v i o r a l a v o i d a n c e o f p h o t o t o x i n s i s a widespread phenomenon; o v e r 70% o f the fauna o f p h o t o t o x i c U m b e l l i f erae i n one study c o n s i s t e d of i n s e c t s f e e d i n g i n a c o n c e a l e d manner (3). Concealed f e e d e r s can e i t h e r be h i g h l y s p e c i a l i z e d (as i s the case f o r umbel l i f e r - f e e d i n g l e a f - m i n i n g Agromyzidae) o r b r o a d l y polyphagous (as i s the case f o r C h o r i s t o n e u r a rosaceana, a t o r t r i c i d l e a f r o l l e r t h a t feeds on a number of p h o t o t o x i c p l a n t s i n the U m b e l l i f erae and i n s e v e r a l o t h e r families). Champagne e t a l . 1986 suggest t h a t , i n a d d i t i o n t o b o r i n g i n t o stems, s p i n n i n g p r o f u s e amounts of s i l k a l s o s e r v e s t o a t t e n u a t e incoming r a d i a t i o n and to p r o t e c t O s t r i n i a n u b i l a l i s , the European c o r n b o r e r , from p h o t o t o x i c a c e t y l e n e s i n i t s h o s t s i n the f a m i l y Compositae. The most c o m p e l l i n g e v i d e n c e f o r a p h o t o p r o t e c t i v e r o l e f o r c o n c e a l e d f e e d i n g i n v o l v e s the i n s e c t fauna o f Hypericum p e r f o r a t u m , St. Johnswort o r Klamath weed. JL^ p e r f o r a t u m c o n t a i n s an extended quinone pigment, h y p e r i c i n , which i s a c t i v a t e d by s u n l i g h t i n t h e r e g i o n o f 500-600 nm (30). A l t h o u g h a p r o p o r t i o n o f the fauna o f St. Johnswort c o n s i s t s o f s p e c i a l i s t s , t h e r e a r e s e v e r a l b r o a d l y polyphagous s p e c i e s t h a t can p r e d i c t a b l y be found f e e d i n g on the f o l i a g e and f l o w e r s ( T a b l e I I I ) . Of t h e s e , one s p e c i e s (a l y c a e n i d c a t e r p i l l a r ) bores i n t o f l o w e r s and f r u i t s , and f i v e ( a l l t o r t r i c i d c a t e r p i l l a r s ) t i e t o g e t h e r l e a v e s , stems o r f l o w e r s and feed i n s i d e these t i e s . O s t e n s i b l y , s i n c e f o l i a g e i s e s s e n t i a l l y opaque t o most w a v e l e n g t h s o f l i g h t , c a t e r p i l l a r s c o n c e a l e d i n l e a f t i e s can feed

210


on p h o t o t o x i c m a t e r i a l w i t h i m p u n i t y ; i n s u f f i c i e n t amounts o f l i g h t p e n e t r a t e to a c t i v a t e the p h o t o t o x i n . When one o f the t o r t r i c i d s , P l a t y n o t a f l a v e d a n a , I s r e a r e d i n the l a b o r a t o r y on an a r t i f i c i a l d i e t , i t cannot engage i n l e a f - t y i n g b e h a v i o r and i s f o r c e d t o feed i n an manner such t h a t i t i s exposed t o l i g h t . C a t e r p i l l a r s r e a r e d on an a r t i f i c i a l d i e t c o n t a i n i n g h y p e r i c i n s u f f e r e d s i g n i f i c a n t l y g r e a t e r m o r t a l i t y when exposed t o f u l l s u n l i g h t than when they were p r o t e c t e d from damaging w a v e l e n g t h s by an a c e t a t e f i l t e r ( T a b l e I V S. Sandberg, i n prep.). L e a f - t y i n g may thus be a p r e a d a p t a t i o n a l l o w i n g g e n e r a l i z e d f e e d e r s , l a c k i n g a s p e c i f i c d e t o x i c a t i o n system f o r p h o t o t o x i n s , t o e x p l o i t p h o t o t o x i c p l a n t s . Such b e h a v i o r may i n f a c t be f a c u l t a t i v e , when P. f l a v e d a n a feeds on the f o l i a g e o f strawberry (Fragaria v i r g i n i e n s i s ) , a nonphototoxic p l a n t , i t o c c a s i o n a l l y spins only a s c a f f o l d i n g of s i l k i n place of a l e a f f o l d i n i t s e a r l y i n s t a r s . Of the r e m a i n i n g l e p i d o p t e r o u s a s s o c i a t e s o f Hypericum, s p e c i e s i n the n o c t u i d genus P o l l a feed n o c t u r n a l l y (G. G o d f r e y , p e r s . comm.), when r i s k s o f p h o t o t o x i c i t y are m i n i m i z e d . N o c t u r n a l l y a c t i v e i n s e c t s i n g e n e r a l may be preadapted f o r f e e d i n g on p h o t o t o x i c p l a n t s . Table I I I . Lepldopteran associates of Hypericum Species

Family

Strymon me11 mis Zale lunata Polla assimllls

31 f l o w e r / f r u i t borer Generallst external f o l l v o r e Generallst 31 31 external f o l l v o r e Salicaeae, Compositae Guttlferae 31 Noctuidae external f o l l v o r e Guttlferae 31 Noctuidae external f o l l v o r e Guttlferae 31 Geometrldae external f o l l v o r e Generallst Geometrldae external f o l l v o r e Generallst Sandberg, in prep.

Delta ramosula Delta stewarti Hyperetls amicarla Eupithecia miserulata Pleuroprucha lnsularia Platynota flavedana Sparganothls sulfureana Xenotemna pallorana Choristoneura parallela Unidentified sp.

Mode of feeding

Ref

Host range

Lycaenidae Noctuidae Noctuidae

Geometrldae external f o l l v o r e

Generallst Sandberg, in prep.

T o r t r l c l d a e leaf tyer T o r t r l c l d a e leaf tyer

Generallst Sandberg, in prep. Generallst Sandberg, in prep.

T o r t r i c i d a e l e a f tyer


T o r t r l c l d a e leaf folder


Graclllarlidae leaf folder

Sandberg, in prep.

Table IV. Effects of hypericin on Placynota flavedana i n the presence and absence of l i g h t (S. Sandberg, i n p r e p a r a t i o n ) 4a. Survivorship (%) of Platynota flavedana to second i n s t a r (n » 40 i n each treatment) Full light Filtered light 1

Control d i e t 0.03% hypericin d i e t

80.0 50.0

85.0 77.5

2 1

A G* test of independence y i e l d e d a value of .109 f o r the Interaction of hypericin and l i g h t regime, i n d i c a t i n g the t o x i c i t y of hypericin i s affected by the l i g h t regime

14.

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211

Resistance to phototoxins Many i n s e c t s may r e l y on p h y s i c a l f a c t o r s f o r p r o t e c t i o n from p h o t o t o x i n s ; i n these c a s e s , a l t h o u g h the i n s e c t i n g e s t s o r c o n t a c t s p h o t o t o x i n s and i s exposed t o l i g h t , the l i g h t f a i l s t o r e a c h the target s i t e of the molecule. I n mammals, d a r k - s k i n n e d i n d i v i d u a l s a r e r e l a t i v e l y more immune t o the e f f e c t s o f i n g e s t i o n o f o r c o n t a c t w i t h p h o t o t o x i n s (32). T h i s r e s i s t a n c e i s a t t r i b u t a b l e t o the d i f f e r e n t i a l concentrations of melanin. M e l a n i n a c t s as a p h o t o p r o t e c t i v e agent i n s e v e r a l ways. M e l a n i n absorbs b o t h UV and v i s i b l e l i g h t and a c t s as a n e u t r a l d e n s i t y f i l t e r ; m e l a n i n c o n t a i n i n g melanosomes s c a t t e r incoming r a d i a t i o n and a t t e n u a t e the l i g h t ; m e l a n i n can absorb r a d i a n t energy and d i s s i p a t e i t as heat; i t can a l s o , as a s t a b l e f r e e r a d i c a l , a c t as a " b i o l o g i c e l e c t r o n exchange polymer" (32). A l t h o u g h much o f the brown o r b l a c k c o l o r a t i o n o f i n s e c t c u t i c l e i s a t t r i b u t a b l e t o t a n n i n g ( i . e . , the protein-quinone c r o s s l i n k a g e i n v o l v e d i n s c l e r o t i z a t l o n ) , dark c o l o r a t i o n i n many s p e c i e s i s due t o d e p o s i t i o n o f m e l a n i n (33). At l e a s t two s p e c i e s o f i n s e c t s a s s o c i a t e d w i t h p l a n t s c o n t a i n i n g p h o t o t o x i n s a r e prone t o m e l a n l c mutations. Melanic l a r v a e of P a p i l i o machaon (the O l d World s w a l l o w t a i l ) , an a s s o c i a t e o f p h o t o t o x i c U m b e l l i f e r a e , a r e known t o o c c u r (34). Manduca s e x t a , the tobacco hornworm ( L e p l d o p t e r a : S p h i n g i d a e ) , feeds on the f o l i a g e of S o l a n a c e a e , I n c l u d i n g L y c o p e r s l c o n e s c u l e n t u m , the tomato, w h i c h i s r e p o r t e d t o c o n t a i n the p h o t o t o x i c furanocoumarin bergapten (35). A mutant form a r i s e s on o c c a s i o n i n which the n o r m a l l y t r a n s p a r e n t c u t i c l e t u r n s b l a c k i n the u l t i m a t e l a r v a l i n s t a r due t o h o r m o n a l l y mediated pigment d e p o s i t i o n (36). These i n d i v i d u a l s can comprise up to 10% o f n a t u r a l p o p u l a t i o n s (G. Kennedy, p e r s o n a l communication 1986). The p h o t o t o x i c f u r a n o c o u m a r i n x a n t h o t o x i n was t o p i c a l l y a p p l i e d i n acetone a t the r a t e o f 50 micrograms/g body weight t o the d o r s a l a r e a o f the t h o r a x o f u l t i m a t e i n s t a r c a t e r p i l l a r s w i t h normal p i g m e n t a t i o n . T h i s treatment i n the presence o f UV l i g h t r e s u l t e d i n major i n j u r y t o t h e pupae. S p e c i f i c a l l y , p u p a l wings f a i l e d t o form and t o s c l e r o t i z e p r o p e r l y . Seventy p e r c e n t o f t h e t r e a t e d i n d i v i d u a l s f a i l e d t o pupate a t a l l o r m a n i f e s t e d c u t i c u l a r damage t o wings. That the damage was e s s e n t i a l l y l i m i t e d t o the d e v e l o p i n g wings i s c o n s i s t w i t h the i n t e r p r e t a t i o n t h a t m i t o t i c a l l y a c t i v e t i s s u e (such as d e v e l o p i n g wing i m a g l n a l d i s c s ) i s p a r t i c u l a r l y s u s c e p t i b l e t o the a n t i m i t o t i c e f f e c t s o f i r r a d i a t e d f u r a n o c o u m a r i n s . When b l a c k mutant hornworm l a r v a e were t r e a t e d i n an i d e n t i c a l f a s h i o n i n t h e u l t i m a t e i n s t a r , o n l y 30% f a i l e d t o pupate o r e x h i b i t e d wing d e f o r m i t i e s (Wiseman and Berenbaum, i n p r e p a r a t i o n ) . M e l a n i n , then, appears t o c o n f e r p r o t e c t i o n a g a i n s t the p h o t o a c t i v a t i o n o f f u r a n o c o u m a r i n s by UV l i g h t and such p r o t e c t i o n may account f o r the p e r s i s t e n t presence o f m e l a n i c i n d i v i d u a l s i n some i n s e c t p o p u l a t i o n s . H i g h l y r e f l e c t i v e s u r f a c e s may a l s o c o n f e r some p r o t e c t i o n a g a i n s t p h o t o t o x i n s (37). S e v e r a l s p e c i e s o f c h r y s o m e l i d b e e t l e s are f r e q u e n t a s s o c i a t e s o f t h e genus Hypericum; o f t h e s e , s p e c i e s i n the genus C h r y s o l l n a a r e c h a r a c t e r i s t i c a l l y m e t a l l i c b l u e - b l a c k i n c o l o r . T h e i r h i g h l y r e f l e c t i v e s u r f a c e may p r e v e n t v i s i b l e l i g h t from e n t e r i n g the body c a v i t y t o a c t i v a t e i n g e s t e d h y p e r i c i n c o n t a i n i n g p l a n t t i s s u e (38). I n g e n e r a l m e t a l l i c c o l o r s , w h i l e


212

a b s o r b i n g i n c i d e n t r a d i a t i o n w e l l , absorb p o o r l y . The m e t a l l i c c u t i c l e o f t i g e r b e e t l e s r e f l e c t s u b s t a n t i a l amounts of shortwave r a d i a t i o n , r a n g i n g from 280 t o 580 nm (39). Biochemical

resistance to

phototoxins

B i o c h e m i c a l r e s i s t a n c e to p h o t o t o x i n s has been documented i n s e v e r a l insects associated with phototoxic plants. Biochemical resistance i n v o l v e s m e t a b o l i s m of a t o x i n such t h a t i t i s no l o n g e r t o x i c . One g e n e r a l b i o c h e m i c a l defense a g a i n s t p h o t o t o x i n s i s to i n t e r c e p t a p h o t o a c t i v e m o l e c u l e w i t h a n o t h e r m o l e c u l e to m a i n t a i n i t i n the o s t e n s i b l y n o n t o x i c ground s t a t e (38). L a r s o n 1986 suggested t h a t many i n s e c t s produce o r s e q u e s t e r c h e m i c a l s w i t h the a b i l i t y to p h y s i c a l l y "quench" e x c i t e d s t a t e s — t h a t i s , to remove energy from an e x c i t e d s t a t e "donor" m o l e c u l e w i t h o u t undergoing s t r u c t u r a l change. Beta c a r o t e n e and r e l a t e d c a r o t e n o i d s , which are e x c e l l e n t quenchers, are widespread i n the hemolymph, wings and integument of h e r b i v o r o u s i n s e c t s (33, 40) and may f u n c t i o n as quenchers f o r those s p e c i e s f e e d i n g on p h o t o t o x i c p l a n t s . In a d d i t i o n , due to i t s a b s o r p t i o n maxima (around 450 t o 550 nm), b e t a c a r o t e n e may d i r e c t l y quench the p h o t o t o x i c f u r a n o c o u m a r i n s , w h i c h show maximal f l u o r e s c e n c e In t h a t r e g i o n . N i t r o g e n - c o n t a i n i n g pigments such as the p t e r i n e s and the ommochromes may a l s o be i n v o l v e d i n oxygen quenching, inasmuch as s i m i l a r a l k a l o i d s possess t h i s p r o p e r t y (41). T o x i c oxygen s p e c i e s are a l s o s u b j e c t to p h y s i c a l and b i o c h e m i c a l d e t o x i c a t i o n i n i n s e c t s t h a t feed on p h o t o t o x i c p l a n t s . C e r t a i n i n s e c t c o n s t i t u e n t s o f c u t i c l e o r hemolymph a r e , o r r e s e m b l e , s t r u c t u r a l l y e f f i c i e n t quenchers of s i n g l e t oxygen. These i n c l u d e c a r o t e n o i d s , amines, and s u l f u r and oxygen d e r i v a t i v e s (38). F l a v o n o i d pigments can a c t as e f f i c i e n t s i n g l e t oxygen s c a v e n g e r s as w e l l . Q u e r c i t i n , a w i d e l y d i s t r i b u t e d p l a n t c o n s t i t u e n t , can suppress s i n g l e t - o x y g e n dependent r e a c t i o n s (42). G l y c o s i d e s o f q u e r c i t i n appear to be s e l e c t i v e l y sequestered from t h e i r f o o d p l a n t s by s w a l l o w t a i l b u t t e r f l i e s i n the t r i b e G r a p h i i n i and by one s p e c i e s i n the genus P a p i l i o (43). P h o t o t o x i c a l k a l o i d s (e.g., b e r b e r i n e ) are r e p o r t e d to occur i n the annonaceous h o s t s of these b u t t e r f l i e s (43) and the u m b e l l i f e r o u s h o s t p l a n t s of P a p i l i o machaon, the s p e c i e s s e q u e s t e r i n g q u e r c i t i n g l y c o s i d e s , are known to c o n t a i n f u r a n o c o u m a r i n s , s e v e r a l of w h i c h g e n e r a t e s i n g l e t oxygen i n the presence o f UV (44). Other s p e c i e s of s w a l l o w t a i l s , p a r t i c u l a r l y i n the T r o i d i n i and P a p i l i o n i n i , s e l e c t i v e l y s e q u e s t e r c a r o t e n o i d s ; o v e r a l l the c o n c e n t r a t i o n of c a r o t e n o i d s i n P a p i l i o n i d a e i s up t o an o r d e r of magnitude h i g h e r than c o n c e n t r a t i o n s i n o t h e r b u t t e r f l y f a m i l i e s ( T a b l e V). R o t h s c h i l d et a l . (45) suggested t h a t c a r o t e n o i d s e q u e s t r a t i o n may s e r v e to p r o t e c t t r o i d i n e s a s s o c i a t e d w i t h A r i s t o l o c h i a c e a e by p r e v e n t i n g f r e e - r a d i c a l o x i d a t i o n of the n i t r o p h e n a n t h r e n e a r i s t o l o c h i c a c i d s to p h e n o l i c s . In a d d i t i o n , c a r o t e n o i d s may s e r v e as s i n g l e t oxygen quenchers f o r the s e v e r a l c l a s s e s of p h o t o s e n s i t i z e r s ( i n c l u d i n g f u r a n o c o u m a r i n s , f u r o q u i n o l i n e a l k a l o i d s , furochromones, and b e n z y l i s o q u i n o l i n e a l k a l o i d s ) present i n the Rutaceae, p r i n c i p a l host f a m i l y f o r the m a j o r i t y o f p a p i l i o n i n e s (46).

14.

BERENBAUM


Table V.

Family Lycaenidae Nymphalidae Pieridae Satyridae Papilionidae*

213

C a r o t e n o i d content o f b u t t e r f l i e s ( 4 0 )

T o t a l ug/g d r y weight 79.4 62.1 32.7 70.4 297

* C a l c u l a t e d from R o t h s c h i l d ( 4 5 ) , Valadon and Mummery (47)

S p e c i f i c b i o c h e m i c a l pathways f o r d e t o x i f i c a t i o n are known t o e x i s t i n some s p e c i e s o f i n s e c t s adapted t o f e e d i n g on p h o t o t o x i c p l a n t s . I v i e and c o l l e a g u e s (48-49) have e x t e n s i v e l y documented t h e m i x e d - f u n c t i o n oxidase-mediated d e t o x i f i c a t i o n o f furanocoumarins by the b l a c k s w a l l o w t a i l P a p i l i o p o l y x e n e s . A l t e r n a t e b i o c h e m i c a l d e t o x i f i c a t i o n systems may e x i s t as w e l l . D e p r e s s a r i a p a s t i n a c e l l a , the p a r s n i p webworm, i s an o e c o p h o r i d c a t e r p i l l a r t h a t feeds e x c l u s i v e l y on the w i l d p a r s n i p , P a s t i n a c a s a t i v a , w h i c h c o n t a i n s s e v e r a l p h o t o t o x i c furanocoumarins (50). T o x i c i t y o f f u r a n o c o u m a r i n s i s not enhanced by mixed f u n c t i o n o x i d a s e i n h i b i t o r s such as t h e m e t h y l e n e d i o x y p h e n y l - c o n t a i n i n g m y r i s t i c i n ( J . N i t a o , i n p r e p a r a t i o n ) ; t h i s o b s e r v a t i o n suggests t h a t an a l t e r n a t e r o u t e i s i n f o r c e . In f a c t , s u b s t a n t i a l amounts o f o r a l l y a d m i n i s t e r e d x a n t h o t o x i n ( a furanocoumarin found i n the p a r s n i p h o s t p l a n t ) a r e r e c o v e r a b l e i n t a c t i n the s i l k and s i l k g l a n d s o f t h e c a t e r p i l l a r , r a i s i n g the p o s s i b i l i t y t h a t the p a r s n i p webworm s e q u e s t e r s p l a n t d e r i v e d p h o t o t o x i n s f o r i t s own defense when ensconced i n l a r v a l webbing o r pupal cocoon s i l k ( J . N i t a o , i n p r e p a r a t i o n ) . Ecological variation To a g r e a t e x t e n t , e c o l o g i c a l f a c t o r s can i n f l u e n c e the e f f i c a c y o f p h o t o t o x i c i t y as a defense a g a i n s t i n s e c t s . On a v e r y s m a l l s c a l e , shade a v a i l a b i l i t y may determine the r e l a t i v e s u s c e p t i b i l i t y o f i n d i v i d u a l p l a n t s I n a p o p u l a t i o n t o i n s e c t s . F o r example, w i l d p a r s n i p s grown under c o n d i t i o n s o f 50 o r 70% ambient l i g h t show a s i g n i f i c a n t r e d u c t i o n i n furanocoumarin c o n t e n t o f t h e f o l i a g e (Berenbaum and Z a n g e r l 1986); inasmuch as furanocoumarins a r e t o x i c t o many i n s e c t s , r e d u c t i o n s i n the f o l i a r c o n c e n t r a t i o n o f these compounds may render p l a n t s i n shady s p o t s more v u l n e r a b l e t o h e r b i v o r y . A l t h o u g h no s p e c i f i c p h o t o t o x i n has been i d e n t i f i e d i n wheat, shade reduces r e s i s t a n c e o f hard r e d s p r i n g wheat t o the wheat stem s a w f l y Cephus c i n c t u s ; i n t h i s case, reduced p h o t o s y n t h e t i c e f f i c i e n c y may have reduced p l a n t v i g o r o r p r o d u c t i o n by t h e p l a n t o f o t h e r d e f e n s i v e c h e m i c a l s (51). S i n c e many a l l e l o c h e m i c a l s a r e induced by l i g h t , v a r i a t i o n i n l i g h t i n t e n s i t y can g r e a t l y a f f e c t t h e c h e m i c a l c o m p o s i t i o n o f above ground p l a n t p a r t s (Berenbaum 1987).

214


Geographic v a r i a t i o n may a f f e c t the e f f i c a c y o f p h o t o t o x i c i t y as a p l a n t defense a g a i n s t i n s e c t s . G l o b a l v a r i a t i o n i n the i n c i d e n c e o f UV and v i s i b l e l i g h t i s s u b s t a n t i a l . T o x i c i t y o f a p h o t o t o x i n can be d i r e c t l y p r o p o r t i o n a l t o UV i n t e n s i t y (Berenbaum and Z a n g e r l 1987), so an e q u i v a l e n t c o n c e n t r a t i o n o f p h o t o t o x i n a t a h i g h e r l a t i t u d e , where i n c i d e n t UV i s a t t e n u a t e d , may have reduced t o x i c i t y . G l o b a l r a d i a t i o n i n t e n s i t y i s determined by a number o f f a c t o r s i n c l u d i n g s o l a r a n g l e , e l e v a t i o n above s e a l e v e l , a t m o s p h e r i c ozone c o n c e n t r a t i o n , atmospheric t u r b i d i t y , degree o f c l o u d c o v e r , and d i s t a n c e to t h e sun a t any p o i n t i n time (52). An i n c r e a s e i n a l t i t u d e from s e a l e v e l t o 4300 m corresponds t o an i n c r e a s e i n UV r a d i a t i o n o f 66% (53). L a t i t u d i n a l d i f f e r e n c e s a l s o a f f e c t UV i n t e n s i t i e s , l a r g e l y due t o g l o b a l d i f f e r e n c e s i n t h e d i s t r i b u t i o n o f atmospheric ozone c o n c e n t r a t i o n s ; g r e a t e r c o n c e n t r a t i o n s o f ozone a t h i g h l a t i t u d e s g r e a t l y reduce the i n t e n s i t y o f b i o l o g i c a l l y e f f e c t i v e UV r a d i a t i o n ( C a l d w e l l 1974). T h i s s o r t o f g l o b a l v a r i a t i o n i n the d i s t r i b u t i o n o f UV r a d i a t i o n may account f o r t h e o b s e r v a t i o n (54) t h a t p l a n t f a m i l i e s w i t h endogenous p h o t o t o x i n s appear t o be more abundant i n r e g i o n s where i n t e n s e s o l a r r a d i a t i o n i s a v a i l a b l e throughout most o f t h e year (e.g., i n t r o p i c a l o r a r i d d e s e r t ecosystems). Conclusions Many p l a n t f a m i l i e s have converged upon a common mechanism o f defense a g a i n s t h e r b i v o r o u s i n s e c t s , t h a t i s , t o e x p l o i t t h e abundant energy a v a i l a b l e i n s u n l i g h t t o p o t e n t i a t e endogenous secondary c h e m i c a l s . I t i s t h e r e f o r e h a r d l y s u r p r i s i n g t h a t , o v e r e v o l u t i o n a r y t i m e , h e r b i v o r o u s I n s e c t s have d e v e l o p e d v a r i o u s and sundry r e s i s t a n c e mechanisms t o these l i g h t - a c t i v a t e d defense compounds. These i n c l u d e b e h a v i o r a l , p h y s i c a l and b i o c h e m i c a l a d a p t a t i o n s t o reduce t h e e x t e n t o f exposure t o e i t h e r the t o x i n o r to p o t e n t i a t i n g w a v e l e n g t h s o f l i g h t , o r t o d i s m a n t l e and d i s a r m the t o x i n i t s e l f . W h i l e l i g h t - a c t i v a t e d p h y t o c h e m i c a l s may w e l l have p o t e n t i a l a p p l i c a t i o n s f o r c o n t r o l purposes i n a g r i c u l t u r a l entomology, these p h y t o c h e m i c a l s may be as prone t o c o u n t e r a d a p t a t i o n by i n s e c t s as a r e the more t r a d i t i o n a l s y n t h e t i c o r g a n i c c o n t r o l c h e m i c a l s — p e r h a p s more so, s i n c e t h e r e a l r e a d y e x i s t s a s u b s t a n t i a l group o f i n s e c t s preadapted t o f e e d i n g on p h o t o t o x i c p l a n t s . M o r e o v e r , t h e r e a r e e c o l o g i c a l c o n s t r a i n t s on the use o f p h o t o t o x i n s f o r widespread i n s e c t c o n t r o l . L o c a l v a r i a t i o n s i n l i g h t regime due t o such u n c o n t r o l l a b l e f a c t o r s as c l o u d c o v e r o r atmospheric t u r b i d i t y , o r t o such u n m o d i f i a b l e f a c t o r s as a l t i t u d e o r l a t i t u d e , may render a s t a n d a r d p h o t o t o x i n based c o n t r o l program a t best u n p r e d i c t a b l e . Acknowledgments I t h a n k E. H e i n i n g e r , R. L a r s o n , J . N e a l , J . N i t a o , and S. S a n d b e r g f o r comments on the m a n u s c r i p t and f o r a l l o w i n g me t o c i t e u n p u b l i s h e d d a t a . T h i s r e s e a r c h was supported by a N a t i o n a l Science Foundation P r e s i d e n t i a l Young I n v e s t i g a t o r Award (NSF BSR 8351407).

14.

BERENBAUM


215

Literature Cited 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24.

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