bk-1983-0208.ch003

3 Impact of Variable Plant Defensive Chemistry on Susceptibility of Insects to Natural Enemies JACK C. SCHULTZ

Downloaded by EAST CAROLINA UNIV on October 2, 2016 | http://pubs.acs.org Publication Date: January 20, 1983 | doi: 10.1021/bk-1983-0208.ch003

Dartmouth College, Department of Biological Sciences, Hanover, NH 03755

The major role of chemical defenses i n plants i s hypothesized to be increasing the impact of insect diseases, parasites, and predators. None of these factors alone provides an explanation of why e v o l u t i o n a r i l y l a b i l e insects rarely defoliate t h e i r long-lived hosts. However, interactions among all of them could increase the useful evolutionary l i f e t i m e of each and the effectiveness of all. In p a r t i c u l a r , chemical v a r i a b i l i t y i s observed to place insects i n compromise situations which increase t h e i r exposure and s u s c e p t i b i l i t y to natural enemies. Forest trees are shown to be highly variable i n space and time, and the impact of t h i s variability on c a t e r p i l l a r s i s explored i n several examples. Despite the impression made by o c c a s i o n a l widespread p e s t outbreaks such as those o f the gypsy moth, severe d e f o l i a t i o n o f f o r e s t e d ecosystems i s q u i t e unusual. Fewer than 10% o f the species l i s t e d i n the Canadian F o r e s t Survey o f L e p i d o p t e r a (1, 2) e x h i b i t p e r i o d i c or o c c a s i o n a l outbreaks. G e n e r a l l y , d e f o l i a t i o n i n f o r e s t s i s l e s s than 7% of primary p r o d u c t i o n p e r year (_3, b u t see 4) . The v a s t m a j o r i t y o f f o r e s t L e p i d o p t e r a a r e q u i t e r a r e almost a l l o f the time, and t h e i r numbers do n o t f l u c t u a t e t o a n o t i c e a b l e degree. These o b s e r v a t i o n s suggest t h a t some f a c t o r o r f a c t o r s normally r e g u l a t e f o r e s t i n s e c t p o p u l a t i o n s and keep d e f o l i a t i o n a t low l e v e l s . A number o f r e g u l a t o r y f a c t o r s have been proposed, and v a r i o u s p o t e n t i a l r e g u l a t o r s have been shown t o operate i n c e r t a i n systems (S,6). However, none o f these f a c t o r s can be shown t o be. g e n e r a l l y e f f e c t i v e i n most o r a l l f o r e s t s . F o r example, a g i v e n p a r a s i t o i d s p e c i e s may be the most important i n f l u e n c e on i t s host a t one s i t e b u t not a t another (7). I t i s d i f f i c u l t t o i d e n t i f y emergent g e n e r a l i z a t i o n s about the r e l a t i v e importance of v a r i o u s p o t e n t i a l c o n t r o l s . 0097-6156/83/0208-0037$06.00/0 © 1983 American Chemical Society

Hedin; Plant Resistance to Insects ACS Symposium Series; American Chemical Society: Washington, DC, 1983.


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PLANT RESISTANCE TO INSECTS

Indeed, e m p i r i c a l o b s e r v a t i o n , e v o l u t i o n a r y theory, and common sense a l l suggest t h a t s i n g l e - f a c t o r approaches are not l i k e l y t o i d e n t i f y u n d e r l y i n g c a u s a l r e l a t i o n s h i p s . Consider the impact of p l a n t defensive chemistry. In recent years i t has become c l e a r t h a t secondary compounds and the r e l a t i v e concentrat i o n s of primary n u t r i e n t s i n p l a n t t i s s u e s may r e s t r i c t f e e d i n g and growth of herbivorous i n s e c t s (see 8 ) . C l e a r l y the a v a i l a b i l i t y of p l a n t t i s s u e s i s a f u n c t i o n of t i s s u e q u a l i t y as w e l l as q u a n t i t y , h e l p i n g t o e x p l a i n why herbivorous i n s e c t s may appear f o o d - l i m i t e d before t h e i r host t i s s u e s are exhausted (9). However, t o maintain f o r e s t i n s e c t p o p u l a t i o n s a t the s t a b l e , extremely low l e v e l s we normally observe, p l a n t chemistry would have t o deter f e e d i n g , poison i n s e c t s , or reduce d i g e s t i o n so s t r o n g l y t h a t p o p u l a t i o n dynamics of the i n s e c t s are profoundly depressed. T h i s n e c e s s i t a t e s d r a s t i c a l l y reducing the f i t n e s s of organisms having enormous p o t e n t i a l f e c u n d i t i e s , p o p u l a t i o n growth r a t e s , and very short generation times. Many f o r e s t Lepidoptera have p o t e n t i a l f e c u n d i t i e s of from 200-1000 eggs/ female, y e t year-to-year p o p u l a t i o n l e v e l s i n d i c a t e s s u r v i v o r ship of only 1 or 2 per female (10). Such a strong impact on s u r v i v o r s h i p or f e c u n d i t y , and on the f i t n e s s of i n d i v i d u a l s , means e x e r t i n g strong n a t u r a l s e l e c t i o n on herbivorous i n s e c t s . T h i s should f a v o r the r a p i d e v o l u t i o n of i n s e c t adaptations which overcome i t . T h i s i s , of course, a common occurrence i n the a p p l i c a t i o n of p e s t i c i d e s or the development of r e s i s t a n t crop p l a n t c u l t i v a r s (11). The s u p p o s i t i o n t h a t p l a n t defenses s e l e c t f o r d e t o x i c a t i o n adaptations i n i n s e c t s i s the foundation of the concept of c o e v o l u t i o n (12). F o r e s t t r e e s represent a p a r t i c u l a r l y v u l n e r a b l e paradox. An i n d i v i d u a l t r e e may l i v e f o r 300 or more years. During t h i s time i t does not move, and presumably cannot adapt t o environmental change. I f t r e e defenses were r e s p o n s i b l e f o r the strong r e g u l a t i o n of i n s e c t s and h e r b i v o r y , the l i f e t i m e of a s i n g l e t r e e ought t o p r o v i d e enough time f o r the e v o l u t i o n of h i g h l y v i r u l e n t i n s e c t s which c o u l d d e f o l i a t e t h e i r host t r e e s repeatedly. T h i s does not appear t o happen. Feeny (13) attempted t o r e s o l v e t h i s dilemma by proposing t h a t f o r e s t t r e e s may have developed a p a r t i c u l a r l y r e c a l c i t r a n t defense, one which even i n s e c t s c o u l d not overcome i n hundreds of generations. H i s suggestion was t h a t protein-complexing p o l y phenols, or t a n n i n s , could p r o v i d e such p r o t e c t i o n . However, there are many i n s e c t s which feed p r e f e r e n t i a l l y on h i g h - t a n n i n content t i s s u e s (14,L5) , and s p e c i f i c adaptations e x i s t which can n u l l i f y or reduce the d i g e s t i o n i n h i b i t i o n e f f e c t s of tannins (16) • One must conclude t h a t no uniform p h y s i c a l or chemical defense should be regarded as insurmountable by e v o l v i n g i n s e c t s . Any uniform chemical p l a n t defense should s e l e c t f o r p e s t s capable of d e f e a t i n g i t . Obviously, however, there i s a s o l u t i o n


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t o t h i s dilemma, s i n c e , as I have p o i n t e d out, f o r e s t s are not s t r i p p e d year a f t e r year.


The E v o l u t i o n a r y Importance of Chemical

Variability

In f a c t , there are a t l e a s t 3 p o s s i b l e s o l u t i o n s . A l l three have one t h i n g i n common: they focus on the r a p i d l y - g r o w i n g body of evidence t h a t t r e e s are not uniform i n defensive chemistry. Instead, most p l a n t s are h i g h l y complex, dynamic mosaics o f v a r i a b l e chemistry and n u t r i e n t v a l u e . T h i s o b s e r v a t i o n suggests ways i n which defensive chemistry may remain e f f e c t i v e over many i n s e c t generations: Complex r e s i s t a n c e . Q u a l i t a t i v e and/or q u a n t i t a t i v e chemical v a r i a t i o n i n p l a n t s may expose i n s e c t s t o more than one d e t e r r e n t (or poison) c o n c u r r e n t l y . S e v e r a l authors have proposed (12^,18,1^) and Pimentel and B e l o t t i (20) have shown i n the l a b o r a t o r y , t h a t i n s e c t s may be slower t o adapt t o such complex chemical mixtures. As a r e s u l t , even s u b l e t h a l doses o f t o x i n s may remain e f f e c t i v e over long p e r i o d s o f time. Resource r e s t r i c t i o n . I f chemical defenses vary q u a n t i t a t i v e l y w i t h i n or between i n d i v i d u a l p l a n t s , then some t i s s u e s may be defended w h i l e others are not. As a r e s u l t , i n s e c t s have a v a i l a b l e t o them the e v o l u t i o n a r y o p t i o n o f avoidance; they may develop the a b i l i t y t o recognize poor q u a l i t y food and a v o i d i t , r a t h e r than e v o l v i n g d e t o x i c a t i o n mechanisms (12,18). T h i s should r e s u l t i n f e e d i n g a c t i v i t y concentrated on a r e s t r i c t e d set o f t i s s u e s or p l a n t i n d i v i d u a l s . There are two important consequences o f t h i s . F i r s t , contact r a t e s w i t h defenses can be lowered by a v o i d i n g them. Hence, the e v o l u t i o n of d e t o x i c a t i o n i s l e s s l i k e l y o r l e s s r a p i d (18). Second, and perhaps more important, the e f f e c t i v e n e s s o f n a t u r a l enemies may be enhanced (below). M u l t i p l e - f a c t o r i n t e r a c t i o n s . Each p o t e n t i a l r e g u l a t o r y f a c t o r may i n t e r a c t s y n e r g i s t i c a l l y w i t h the others and enhance t h e i r e f f e c t i v e n e s s . For example, p l a n t chemistry can i n f l u e n c e the e f f e c t i v e n e s s of p r e d a t o r s , p a r a s i t o i d s and diseases i n a v a r i e t y of ways (_21,J22,23) . However, the s e l e c t i v e pressure exerted by uniform chemical defenses should be strengthened by i n t e r a c t i o n s w i t h n a t u r a l enemies, and t h e i r u s e f u l l i f e w i l l be shortened. Consequently, although the ways i n which p l a n t chemistry can i n f l u e n c e the e f f e c t i v e n e s s o f n a t u r a l enemies are d i z e r s e , they can remain e f f e c t i v e through e v o l u t i o n a r y time only i f v a r i a b i l i t y i s p a r t o f the p i c t u r e as w e l l . I n f a c t , although reviews have tended t o focus on chemical enhancement o f n a t u r a l enemy r e g u l a t i o n (23), there are probably as many ways i n which uniform p l a n t chemistry can i n t e r f e r e w i t h the a c t i o n s o f these enemies as there



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are p o s i t i v e e f f e c t s (24,25,26). I t i s not even c l e a r t h a t the impact o f uniform p l a n t defenses w i l l always be p o s i t i v e from the p l a n t ' s p o i n t o f view. I suggest t h a t v a r i a b l e p l a n t chemistry, by r e s t r i c t i n g resource a v a i l a b i l i t y and f o c u s i n g the a c t i v i t i e s of herbivores on a few t i s s u e s , promotes compromises between f o o d - f i n d i n g and r i s k s from n a t u r a l enemies which are n o t r e a d i l y countered by most i n s e c t s . The s p a t i a l and temporal heterogeneity which appears t o be common i n f o r e s t t r e e s i s the most important p a r t of the t r e e ' s defensive system, and i s the only way a p l a n t ' s chemical defenses can remain e f f e c t i v e over e v o l u t i o n a r y time. T h i s v a r i a b l e impact on n a t u r a l enemies may be more important i n r e g u l a t i n g consumption than any s i n g l e f a c t o r can be. V a r i a b i l i t y i n Tree Defenses There are many p o s s i b l e causes of chemical and n u t r i e n t v a r i a b i l i t y i n t r e e t i s s u e s (27,28) which r e s u l t i n a wide range of s p a t i a l a r r a y s o f s u i t a b l e and u n s u i t a b l e food f o r i n s e c t s (29). Although l a r g e - s c a l e s p a t i a l v a r i a t i o n may i n f l u e n c e i n s e c t host race formation and have i n t e r e s t i n g consequences f o r i n s e c t biogeography and host race formation (30), the s c a l e o f v a r i a t i o n w i t h which the i n d i v i d u a l i n s e c t deals most o f t e n i s more l o c a l , on the i n d i v i d u a l t r e e or t i s s u e b a s i s . Most a n t i h e r b i v o r e t r a i t s have been found t o be h i g h l y v a r i a b l e on t h i s smaller s c a l e ; s i g n i f i c a n t v a r i a t i o n i n n u t r i e n t content and secondary chemistry i s commonly observed w i t h i n t r e e canopies, on a branch-to-branch b a s i s (28,29). On an even f i n e r s c a l e , we have found t h a t adjacent leaves on s i n g l e sugar maple (Acer saccharum Marsh) and y e l l o w b i r c h (Betula a l l e g h e n i e n s i s B r i t t . ) may d i f f e r g r e a t l y i n s e v e r a l t r a i t s important t o herbivorous i n s e c t s (31; F i g u r e 1). Some o f these d i f f e r e n c e s , e.g., i n tanning c o e f f i c i e n t (32), vary by f a c t o r s o f 2 o r more from l e a f t o l e a f (Figure 1). The p a t t e r n o f such v a r i a t i o n appears random i n sugar maple, b u t may be ager e l a t e d and hence s p a t i a l l y p r e d i c t a b l e (young leaves occur only a t c e r t a i n growing p o i n t s ) i n yellow b i r c h (31). I n s e c t s such as c a t e r p i l l a r s f o r a g i n g along sugar maple branches may have l i t t l e i n f o r m a t i o n a v a i l a b l e t o them about the s p a t i a l d i s t r i b u t i o n o f l e a f q u a l i t y , w h i l e those f o r a g i n g i n y e l l o w b i r c h may be able t o l o c a t e leaves w i t h p a r t i c u l a r t r a i t s by searching i n c e r t a i n p l a c e s -{e.g., ends o f branches). The s i g n i f i c a n c e o f such s p a t i a l a r r a y s l i e s i n the b e h a v i o r a l responses of i n s e c t s f o r a g i n g i n these t r e e s . I f c e r t a i n l e a f types a r e u n a v a i l a b l e w h i l e others a r e p r e f e r r e d , then such s p a t i a l arrays f o r c e i n s e c t s t o move about i n search of good feeding s i t e s (29). For i n s e c t s which spend much time (or a l l o f t h e i r l i v e s ) feeding i n one p l a c e ( s e s s i l e s p e c i e s , such as a p h i d s ) , t h i s search i s performed once; a f t e r a s u i t a b l e s i t e i s l o c a t e d , these i n s e c t s a r e r e s t r i c t e d t o one p o r t i o n o f t h e i r



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TOUGHNESS g/cm

12.0-I

2

•mm una u Vi^174.75 m ntiii mmm 12.0

V ; ^ W / ; # V ; | ^ 97.75 WATER

J 64.48 m 'll.JMtMMIk

70.75

POLYPHENOLS V. TAE 0.03 0.177

045 0.03 TANNING % TAE

0.340

LEAF

A B

C D E

A

B C D E

Figure 1. Leaf-to-leaf variation in four traits along a single branch of sugar maple (left) and yellow birch (right) on 6/23/81. Horizontal axis is mean of each measure for that branch; hatched area is one standard deviation. Each black bar represents the actual value for one leaf, plotted as deviation from the mean. Branch terminus is to right; yellow birch leaves D and E are at least 10 days younger than the others.



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h o s t s . More mobile species which r e q u i r e more food t o complete development (e.g., c a t e r p i l l a r s ) must repeatedly search f o r new feeding s i t e s throughout t h e i r l i v e s . Many i n s e c t s do indeed recognize and respond t o t i s s u e q u a l i t y v a r i a t i o n . There are numerous examples o f l e a f - a g e s p e c i f i c preferences among f o l i v o r o u s i n s e c t s , i n c l u d i n g some which make r i g i d feeding d e c i s i o n s based on t i s s u e ages which d i f f e r by l e s s than a few weeks (29). The apparent r e s i s t a n c e o f i n d i v i d u a l t r e e s i n otherwise s u s c e p t i b l e stands has been recogn i z e d f o r some time (e.g., 33). The few species o f Lepidoptera l a r v a e whose f o r a g i n g behavior has been s t u d i e d t r a v e l c o n s i d e r able d i s t a n c e s (sometimes s e v e r a l meters) and spend l a r g e p r o p o r t i o n s o f t h e i r time sampling, r e j e c t i n g and judging the a c c e p t i b i l i t y o f leaves on i n d i v i d u a l host t r e e s (29). G a l l forming aphids s e l e c t leaves o f a c e r t a i n s i z e and may engage i n t e r r i t o r i a l d i s p u t e s t o p r o t e c t t h e i r choices (34). I t appears c l e a r t h a t i n d i v i d u a l i n s e c t s respond t o s p a t i a l v a r i a b i l i t y i n f o r e s t t r e e leaves. Temporal v a r i a b i l i t y i n t r e e t i s s u e q u a l i t y i s w e l l known (see _29r.35 f o r review) . Year-to-year, seasonal, day-to-day, and d i u r n a l s h i f t s i n n u t r i e n t contents and secondary chemistry have a l l been observed. P a r t i c u l a r l y i n t r i g u i n g i s the i n c r e a s i n g body o f evidence t h a t damage by i n s e c t s and pathogens may r e s u l t i n short-term o r year-to-year changes i n secondary chemistry (36, 32). We have found t h a t ongoing d e f o l i a t i o n by gypsy moth (Lymantria d i s p a r L.) l a r v a e i s a s s o c i a t e d w i t h profound changes i n p h e n o l i c chemistry o f red oak (Quercus rubrum) leaves (38). Over a p e r i o d o f a month, tanning c o e f f i c i e n t s increased d r a m a t i c a l l y , and seasonal (2 month) i n c r e a s e s i n h y d r o l y z a b l e tannins were observed i n t r e e s undergoing d e f o l i a t i o n . P r e l i m i n a r y s t u d i e s o f y e l l o w b i r c h and sugar maple suggest t h a t dayto-day responses i n p h e n o l i c p r o d u c t i o n may be generated by damage t o leaves (39)• The importance o f seasonal changes i n secondary chemistry and n u t r i e n t s t o the feeding success and l i f e h i s t o r y p a t t e r n s o f some f o r e s t Lepidoptera i s w e l l e s t a b l i s h e d (40,41). Year t o year changes i n chemical phenology may i n f l u e n c e t r e e s u s c e p t i b i l i t y and i n s e c t p o p u l a t i o n dynamics (42,43). Hence, a given t r e e may not present the same d i s t r i b u t i o n o f l e a f q u a l i t y i n every year. I n s e c t s attempting t o assess host q u a l i t y f o r o f f s p r i n g which w i l l feed d u r i n g the next year o r even l a t e r i n the same season may not have very complete i n f o r m a t i o n a v a i l a b l e f o r selecting oviposition sites. Shorter-term temporal v a r i a t i o n i n l e a f q u a l i t y should a c t t o complicate the s p a t i a l a r r a y s d e s c r i b e d above. Thus, not only may a f o r a g i n g i n s e c t have d i f f i c u l t y l o c a t i n g s u i t a b l e feeding s i t e s i n space, but t h e i r l o c a t i o n s may s h i f t from time t o time o r c o n t i n u o u s l y , as seasonal changes, i n d u c t i o n e f f e c t s , o r even p l a n t pathogen a t t a c k (44) a l t e r t i s s u e q u a l i t y . A s u i t a b l e t i s s u e a t one time may not be s u i t a b l e l a t e r i n the day, o r l a t e r i n the i n s e c t ' s l i f e .



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The p i c t u r e o f a f o r e s t t r e e t h a t I wish t o p o r t r a y , then, i s one o f great s p a t i a l h e t e r o g e n e i t y , complicated by ongoing change. For an i n s e c t capable o f d e a l i n g w i t h some subset o f the great number o f t i s s u e q u a l i t y f a c t o r s which could i n f l u e n c e f e e d i n g , there may be only a l i m i t e d a r r a y o f s u i t a b l e t i s s u e s i n a canopy. These s u i t a b l e s i t e s may be w i d e l y s c a t t e r e d , f o r c i n g long searches and much t r a v e l i n g . The p a t t e r n i s complicated f u r t h e r by c o n s t a n t l y changing t i s s u e q u a l i t i e s . The s i t u a t i o n can be s a i d t o resemble a " s h e l l game", i n which a v a l u a b l e resource ( s u i t a b l e leaves) i s "hidden" among many other s i m i l a r - a p p e a r i n g but u n s u i t a b l e resources. The i n s e c t must sample many t i s s u e s t o i d e n t i f y a good one. The l o c a t i o n o f good t i s s u e s may be s p a t i a l l y u n p r e d i c t a b l e , and may even change w i t h time. For a "choosy" o r d i s c r i m i n a t i n g i n s e c t , f i n d i n g s u i t a b l e food i n an apparently uniform canopy c o u l d be h i g h l y complex. Impact on N a t u r a l Enemies Although chemical v a r i a b i l i t y may not a l t e r a l l o f the p o t e n t i a l e f f e c t s o f p l a n t chemistry on the e f f e c t i v e n e s s o f n a t u r a l enemies, there are a number o f important q u a l i t a t i v e d i f f e r e n c e s i n the k i n d s o f i n t e r a c t i o n s p o s s i b l e . I n some cases the impact v a r i a b l e chemistry may have on an i n s e c t ' s s u s c e p t i b i l i t y t o r i s k s i s simply g r e a t e r than i t would be were p l a n t chemistry uniform. I n other cases w h o l l y d i f f e r e n t r e l a t i o n s h i p s are p o s s i b l e . T o x i c substances a c q u i r e d from the host p l a n t may p r o v i d e r e s i s t a n c e t o p a r a s i t o i d s (24), pathogens (25), and predators (45). By a v o i d i n g some t o x i n s i n p l a n t m a t e r i a l and s e l e c t i n g s u p e r i o r food t i s s u e s , i n s e c t s feeding on v a r i a b l e hosts may become more s u s c e p t i b l e t o some enemies. Of course, other substances i n p r e f e r r e d t i s s u e s may s t i l l be t o x i c t o c e r t a i n o f these enemies, but t h i s i s l e s s l i k e l y than i t would be were p l a n t compounds u n i f o r m l y encountered by the host i n s e c t . An i n s e c t host's exposure t o p a r a s i t e s and predators may be increased by v a r i a b l e p l a n t defenses i n three ways. F i r s t , by r e s t r i c t i n g f e e d i n g a c t i v i t y t o c e r t a i n t i s s u e types o r p o r t i o n s of the host p l a n t , the p o s i t i o n o f i n s e c t hosts becomes more p r e d i c t a b l e . P a r a s i t e s (24,46,42) o r predators (48) able t o recognize p h y s i c a l p l a n t t r a i t s such as t i s s u e c o l o r o r form, o r those capable o f employing the unique chemistry o f the p r e f e r r e d t i s s u e s as cues (47,49) would be able t o l o c a t e t h e i r hosts more r e a d i l y by f o c u s i n g t h e i r search on these t r a i t s . Second, the increased movement necessary f o r l o c a t i n g w i d e l y d i s p e r s e d feeding s i t e s should i n c r e a s e contact r a t e s w i t h enemies. Movement makes i n s e c t s more conspicuous t o p a r a s i t o i d s or predators s e n s i t i v e t o i t (50,51). Random encounters w i t h arthropod predators o r p a r a s i t e s should i n c r e a s e w i t h searching a c t i v i t y , as would r i s k o f dislodgement and f a l l o u t .



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Moving long d i s t a n c e s and t a s t i n g many s u r f a c e s (29) may a l s o g r e a t l y i n c r e a s e contact r a t e s w i t h pathogens. Pathogens are o f t e n d i s t r i b u t e d on p l a n t t i s s u e s u r f a c e s by other host i n s e c t s (52), and are t r a n s m i t t e d by subsequent contact w i t h the same s u r f a c e s . Increased movement should d i s p e r s e pathogens more w i d e l y and i n c r e a s e the p r o b a b i l i t y of encountering them. Moreover, the chemistry of p l a n t t i s s u e s may i n f l u e n c e the composition of t h e i r surface f a u n a s / f l o r a s (53). Hence, by f o c u s i n g f e e d i n g a c t i v i t i e s on t i s s u e s w i t h c e r t a i n chemical t r a i t s , i n s e c t s may simultaneously f i n d themselves feeding on t i s s u e s which promote the growth of pathogens. T h i s may be p a r t i c u l a r l y important when l e a f age i s a c r i t e r i o n f o r c h o i c e . We have observed c o n s i s t e n t l y e l e v a t e d v i r a l m o r t a l i t y (70% vs 30%, N = 80) among i n d i v i d u a l s of the n o c t u i d , O r t h o s i a h i b i s c i Guenee, when fed o l d e r (45 days) y e l l o w b i r c h leaves as compared w i t h those fed young ( l e s s than 10 days) leaves from the same t r e e . Although t h i s e f f e c t could be due t o d i f f e r e n t i a l chemistry i n the two l e a f age c l a s s e s (31), a more parsimonious hypothesis i s t h a t o l d e r leaves have had more time t o c o l l e c t more pathogens. Hence, t r a v e l l i n g on o l d e r leaves may be q u i t e r i s k y . Some i n s e c t species may avoid the r i s k s of cuing v i s u a l predators (e.g., b i r d s ) w h i l e moving by being a c t i v e only a t n i g h t (29,54). I n many h a b i t a t s t h i s would mean reducing the time a v a i l a b l e f o r feeding by one-half or t w o - t h i r d s , r e s u l t i n g i n a decrease i n growth r a t e of as much as 40 or 50% (_55,56) . Slowing the growth r a t e by t h i s much adds to the l e n g t h of time an i n s e c t i s a v a i l a b l e t o a l l r i s k s (57,58); there i s a t r a d e o f f between r e s t r i c t e d feeding and r i s k s over the l i f e t i m e of the i n s e c t as w e l l as d u r i n g each feeding bout. T h i s i s the t h i r d means by which the i n s e c t ' s exposure t o r i s k s i s increased by v a r i a b l e host q u a l i t y . These t r a d e o f f s can be d e p i c t e d g r a p h i c a l l y (Figure 2 ) . I have suggested (29) t h a t the form of expected food y i e l d d u r i n g an i n s e c t ' s f o r a g i n g among v a r i a b l e resources should be r e p r e sented by a r i s i n g , asymptotic curve i f the i n s e c t s e l e c t s some subset of t i s s u e s from those i t encounters. We can p l o t the s u r v i v o r s h i p p r o b a b i l i t y of an i n d i v i d u a l as a negative expon e n t i a l f u n c t i o n of the capture r a t e ; such a f u n c t i o n f o r a constant capture r a t e of 30% i s shown i n F i g u r e 2. A capture r a t e of 30% represents the median r a t e of removal of c a t e r p i l l a r s by b i r d s i n a n o r t h temperate f o r e s t as determined by Holmes e t a l (59), and i s a c o n s e r v a t i v e estimate f o r p a r a s i t i s m r a t e s a t moderate host d e n s i t i e s (e.g. 60). The more v a r i a b l e the leaves from which an i n s e c t must s e l e c t a meal, the lower i t s expected y i e l d over a given time i n t e r v a l (the lower y i e l d curve i n F i g u r e 2 represents 1/2 the a v a i l a b l e leaves of the upper curve, or t w i c e the v a r i a b i l i t y ) . As a r e s u l t of the increased time spent s e a r c h i n g , the contact r a t e w i t h and p r o b a b i l i t y of capture by a predator o r p a r a s i t e i n c r e a s e s g r e a t l y f o r a given food y i e l d as t i s s u e s become more v a r i a b l e . There i s a d i r e c t i n f l u e n c e of v a r i a b i l i t y on r i s k .



\

N

30%

TIME

Mortality

OR

Variable

DISTANCE

Less

Figure 2. Graphical model of yield and risk accruing during foraging by a defoliating insect. Mortality from natural enemies is assumed to be constant at 30%, resulting in exponentially decreasing survivorship curve (dashed). Yield (solid lines) accumulates curvilinearly (see 29) and more rapidly when leaves are less variable (because most leaves can be consumed) than when they are highly variable (many do not contribute to the diet). For an expected yield of 1 hypothetical unit, foraging longer (because leaves are variable) reduces the probability of surviving by an amount labeled E(Y)=1 on right axis. The reduction in survivorship is much greater by the time E(Y)—2. Leaf variability decreases the probability of surviving.

\



46


An example employing data f o r gypsy moth l a r v a e and t h e i r t a c h i n i d f l y p a r a s i t e , B l e p h a r i n a p r a t e n s i s Meigen, i s d e p i c t e d i n F i g u r e 3. The p a r a s i t o i d i n f e c t i o n r a t e i s d e r i v e d from s t u d i e s done i n Centre County, PA, under moderate gypsy moth d e n s i t i e s (60). The f l i e s begin t o o v i p o s i t on f o l i a g e when gypsy moth l a r v a e are i n the 3d i n s t a r , and the microtype eggs are consumed by l a r v a e . There i s d i f f e r e n t i a l p a r a s i t o i d s u r v i v o r s h i p i n c a t e r p i l l a r s of d i f f e r e n t i n s t a r s , and the " s u r v i v a l " curve i n F i g u r e 3 represents s u c c e s s f u l c a t e r p i l l a r k i l l s c o r r e c t e d f o r p a r a s i t o i d m o r t a l i t y i n the host. C a t e r p i l l a r dry weights are taken from a study (61) of the e f f e c t s of gypsy moth d e f o l i a t i o n on host p l a n t food q u a l i t y and l a r v a l growth. The "normal f o l i a g e " growth curve approximates the growth r a t e of gypsy moth l a r v a e on normal oak f o l i a g e through the l a s t 4 i n s t a r s . The "induced f o l i a g e " curve approximates the growth of l a r v a e on f o l i a g e from d e f o l i a t e d t r e e s (61). Development time f o r these l a r v a e i s about 4 days (3-4%) longer than i t i s f o r "normal f o l i a g e " l a r v a e (61). Most of the r e t a r d a t i o n occurs i n the f i r s t 3 i n s t a r s ; by" the 5th and 6th i n s t a r s reduced food q u a l i t y no longer depresses growth r a t e s below c o n t r o l l a r v a e (M. Montgomery, pers. comm.). As a consequence of an apparently induced change i n food q u a l i t y (probably due to increased t a n n i n contents; _38), development time i s lengthened. T h i s i n t u r n r e s u l t s i n an increase i n p a r a s i t i s m r a t e s . The d e p i c t i o n i n F i g u r e 3, although somewhat schematic, shows a decrease i n s u r v i v o r s h i p of almost 20% r e s u l t ing from a growth r a t e r e d u c t i o n of 3%. I n t e r e s t i n g l y , were growth r a t e s slowed enough, the c a t e r p i l l a r s could escape p a r a s i t i s m by t h i s f l y . B. p r a t e n s i s eggs l a s t about 2 weeks on f o l i a g e . Were development of some c a t e r p i l l a r s delayed enough, they might enter the 3d i n s t a r l a t e enough t o avoid v i a b l e p a r a s i t o i d eggs. On the other hand, the a d u l t f l i e s apparently t r a c k c a t e r p i l l a r p o p u l a t i o n development and time o v i p o s i t i o n t o c o i n c i d e w i t h entry i n t o the 3d c a t e r p i l l a r i n s t a r (60). Thus a constant m o r t a l i t y or s u s c e p t i b i l i t y , from a complex of enemies or from g e n e r a l i z e d predators or p a r a s i t e s , r e s u l t s i n a steep i n c r e a s e i n r i s k w i t h time vFigure 2). The time necessary t o accumulate m a t e r i a l s f o r growth and the l e v e l of r i s k w h i l e doing so may be increased g r e a t l y when food p l a n t q u a l i t y i s v a r i a b l e . Both s p a t i a l v a r i a b i l i t y and temporal v a r i a b i l i t y (e.g. induction) can have t h i s e f f e c t . Even when the r i s k accumulation i s slower and growth i s slowed a very small amount (as i n the f l y - g y p s y moth c a s e ) , host p l a n t v a r i a t i o n can have a major impact on exposure t o enemies (Figure 3). F i n a l l y , density-dependent m o r t a l i t y from v a r i o u s enemies may be enhanced by host p l a n t v a r i a t i o n . Again, f o c u s i n g feeding a c t i v i t i e s on a r e s t r i c t e d set of s u i t a b l e t i s s u e s should a l s o focus the a c t i v i t i e s and abundance of pathogens, p a r a s i t o i d s , and predators. S e s s i l e i n s e c t s , such as g a l l - f o r m i n g aphids (55,62),



Figure 3. Relationship between growth rate of gypsy moth larvae on "normal" and "induced" foliage and mortality due to the tachinid parasite, Blepharina pratensis. Larvae grow more slowly on induced foliage and are exposed to parasitism longer. A given larval weight, X, is attained later on induced foliage, so that infection rates are higher. Hatched area accounts for larval-age specific mortality of B . pratensis; upper "survival" curve is corrected survival curve for infected larvae. In this case, a 3% decrease in growth of gypsy moth larvae results in an approximately 20% decrease in survivorship. See text for details.



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experience increased contagion i n terms of m o r t a l i t y from enemies. By o c c u r r i n g p r e d i c t a b l y on p a r t i c u l a r p l a n t surfaces or i n p a r t i c u l a r l o c a t i o n s , i n s e c t s may focus the searching a c t i v i t i e s of predators and p a r a s i t e s i n a density-dependent f a s h i o n (e.g., 55,62,63). More complex, second order i n t e r a c t i o n s may be imagined, i n v o l v i n g more than one n a t u r a l enemy. For example, consider i n s e c t s t o which tannins are important d e t e r r e n t s and d i g e s t i o n i n h i b i t o r s . As mentioned above, e l e v a t e d gut pH appears to be a way of d e a l i n g w i t h t a n n i n s , since t a n n i n - p r o t e i n complexes are d i s s o c i a t e d or i n h i b i t e d a t a l k a l i n e pH (16,32). Indeed, u s i n g a model i n v i t r o system i n which hemoglobin i s employed as a p r o t e i n s u b s t r a t e , we found t h a t s e v e r a l n a t u r a l tannins and p h e n o l i c e x t r a c t s do not p r e c i p i t a t e t h i s p r o t e i n when the pH exceeds about 8.5 (Figure 3; 32); b i n d i n g i s q u i t e complete from pH 4 through 8. Although hemoglobin i s not a p l a n t p r o t e i n , i t resembles s e v e r a l p l a n t p r o t e i n s i n molecular s i z e and s o l u b i l i t y ( u n l i k e c a s e i n , f o r example) and i s a u s e f u l comparison (32). I t i s i n t e r e s t i n g t o note t h a t the s o l u b i l i t y of the c r y s t a l l i n e t o x i n of a common, important c a t e r p i l l a r pathogen, B a c i l l u s t h u r i n g i e n s i s ( B t ) , runs from j u s t over pH 8 to about pH 9.5 (64,65,66). Above pH 9.5, there i s some doubt t h a t the p r o t e i n t o x i n remains e f f e c t i v e (66). Hence, a c a t e r p i l l a r adapted f o r feeding on h i g h - t a n n i n foods i s i n a p r e c a r i o u s s i t u a t i o n , caught between i n c r e a s i n g the d i g e s t i b i l i t y of i t s food and the r i s k of pathogen " s u s c e p t i b i l i t y . The s o l u b i l i t y of the p r o t e i n coats of s e v e r a l nuclear p o l y h e d r o s i s v i r u s e s (NPV)- and hence t h e i r v i r u l e n c e i n the i n s e c t gut- ranges from pH 4.5 t o pH 8.5 (67,68). Hence t a n n i n - t o l e r a n t i n s e c t s w i t h e l e v a t e d gut pH's may be r e l a t i v e l y r e s i s t a n t t o these pathogens. According t o theory (6£,70), e a r l y s u c c e s s i o n a l p l a n t s should have low t a n n i n contents and t h e i r herbivores should have lower gut pH values (16). An emerging hypothesis would be t h a t c a t e r p i l l a r species feeding on l a t e s u c c e s s i o n a l t r e e s would be more s u s c e p t i b l e t o Bt and l e s s s u s c e p t i b l e t o NPV than are t h e i r r e l a t i v e s on e a r l i e r s u c c e s s i o n a l p l a n t s . T h i s hypothesis i s as yet untested. It could have great p r a c t i c a l importance, since these pathogens are c u r r e n t l y being developed and promoted as b i o l o g i c a l c o n t r o l agents f o r f o r e s t pests on both h i g h - t a n n i n and low-tannin t r e e species. M i c r o b i a l c h i t i n a s e has been proposed as a s y n g e r g i s t f o r Bt (71). I t s r o l e would be t o d i g e s t holes i n the i n s e c t gut w a l l and f a c i l i t a t e p e n e t r a t i o n of Bt t o x i n . However, unless the c a t e r p i l l a r ' s gut pH can be manipulated (71), t h i s i s u n l i k e l y t o be e f f e c t i v e w i t h B t , but might be f e a s i b l e w i t h NPV (Figure 4 ) . How does chemical v a r i a b i l i t y enter i n t o t h i s pH scenario? F i r s t , by c o n c e n t r a t i n g on low-tannin t i s s u e s , an i n s e c t may be able t o feed on a t r e e species w i t h h i g h average t a n n i n values w h i l e m a i n t a i n i n g a lower gut pH. However, t h i s could i n c r e a s e pathogen r i s k (Figure 4 ) . Second, gut pH may f l u c t u a t e w i t h the



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Figure 4. Binding of a protein (hemoglobin) to several tannin extracts (tannic acid, sugar maple tannins, yellow birch tannins, quebracho tannins; see 29) at various pH values. Ranges of microbial chitinase activity, NPV activity, and Bt toxicity are given. See text for discussion and references.


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50


food a c t u a l l y i n g e s t e d , and may decrease i n animals starved f o r 12 hours (72). Thus any i n s e c t e x p e r i e n c i n g long p e r i o d s between meals may experience lowered gut pH and p o s s i b l e d i g e s t i b i l i t y problems when feeding begins. More i n t e r e s t i n g , a high gut pH may d e c l i n e i n t o a r e g i o n of maximum p a t h o g e n i c i t y f o r organisms l i k e Bt. But why would a c a t e r p i l l a r not feed f o r up t o 12 hours? I f s u i t a b l e food i s widely s c a t t e r e d and r i s k s of movement among f e e d i n g s i t e s are h i g h (above), many i n s e c t s may be forced t o feed only a t n i g h t (29,54). In north temperate f o r e s t s , such an i n s e c t w i l l " s t a r v e " f o r from 8 t o 14 hours. One consequence of t h i s t a c t i c may be t h a t the f i r s t meal of the evening may be very risky. Some aspects of p l a n t v a r i a t i o n could i n t e r f e r e w i t h the impact of n a t u r a l enemies. Some enemies may be unable t o a s s o c i ate m i c r o h a b i t a t cues (e.g., chemical, p h y s i c a l , c o l o r , p o s i t i o n ) w i t h prey or host l o c a t i o n . For these enemies, prey or host f e e d i n g on r e s t r i c t e d t i s s u e s w i l l tend t o appear widely spaced and they may not be r e a d i l y encountered. I t appears t o me t h a t many, i f not most, p a r a s i t o i d s and predators can be found t o use one o r more cues. T h i s negative e f f e c t could be counteracted by i n c r e a s e d encounter r a t e s d u r i n g h e r b i v o r e searching movements. The metabolic c o s t s of t r a v e l l i n g among feeding s i t e s and r e s t i n g long p e r i o d s without feeding could be t r a n s l a t e d d i r e c t l y i n t o reduced i n s e c t f e c u n d i t y (29). Were t h i s e f f e c t strong enough, i t i s conceivable t h a t i n s e c t d e n s i t i e s might be reduced d i r e c t l y . A p o s s i b l e consequence of t h i s would be reduced density-dependent m o r t a l i t y . There are no data a v a i l a b l e f o r the metabolic c o s t s of 'walking f o r i n s e c t s such as c a t e r p i l l a r s . Conclusions and Management Prospects I have argued t h a t uniform chemical defenses cannot be e v o l u t i o n a r i l y s t a b l e . For t r e e s , t h i s means they should not remain e f f e c t i v e even f o r a s i n g l e t r e e generation. But t r e e s are not uniform; they are dynamic, h i g h l y d i v e r s e h a b i t a t s and food sources f o r i n s e c t s . Although p l a n t chemistry can i n f l u e n c e n a t u r a l enemies d i r e c t l y , i t may do so i n e i t h e r p o s i t i v e o r negative f a s h i o n , and t h i s i n f l u e n c e should not remain e f f e c t i v e over e v o l u t i o n a r y time, e i t h e r . However, chemical v a r i a b i l i t y i n f l u e n c e s s u s c e p t i b i l i t y of h e r b i v o r e s t o n a t u r a l enemies by f o r c i n g c o s t l y t r a d e o f f s upon i n s e c t s which i n v o l v e unavoidable r i s k s and metabolic c o s t s . These d i f f i c u l t i e s are l e s s e a s i l y overcome by adaptation. I n a d d i t i o n t o these s y n e r g i s t i c e f f e c t s , chemical v a r i a b i l i t y could maintain the e f f e c t i v e n e s s of p l a n t defenses through a general slowing of adaptation due to lowered contact r a t e s w i t h s p e c i f i c defenses or the d i f f i c u l t y of d e a l i n g with multiple factors. These observations are of p r a c t i c a l importance. The k i n d s of v a r i a b i l i t y I have d e s c r i b e d appear t o e x e r t c o n t r o l on i n s e c t



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p o p u l a t i o n s and consumption i n nature. For example, i n d u c t i o n responses may be c r i t i c a l t o l i m i t i n g o c c a s i o n a l pest outbreaks (35,36,38). The t i m i n g and type o f human i n t e r v e n t i o n i n such events c o u l d d i s r u p t such d e l i c a t e c o n t r o l s . E a r l y r e d u c t i o n i n i n s e c t d e n s i t i e s d u r i n g an outbreak through the use o f p e s t i c i d e s or a b i o l o g i c a l c o n t r o l agent a c t i n g e a r l y i n the l i f e h i s t o r y o f a p e s t l i k e the gypsy moth c o u l d reduce the impact o f c a t e r p i l l a r feeding on host t r e e s and slow o r h a l t t r e e i n d u c t i o n responses. J u s t such a s i t u a t i o n , although w i t h l i t t l e c o n s i d e r a t i o n o f the b i o l o g y o f the p a r t i c i p a n t s , has been modelled by s e v e r a l authors (73,74). As a r e s u l t o f untimely i n t e r v e n t i o n , i n t e r a c t i o n s which may n a t u r a l l y l i m i t outbreaks c o u l d be f r u s t r a t e d and a r t i f i c i a l c o n t r o l s may become necessary over extended p e r i o d s . Some b i o l o g i c a l c o n t r o l e f f o r t s may be f a u l t y or may be improved when p l a n t chemistry and v a r i a b i l i t y are taken i n t o account. For example, i t seems reasonable t o hypothesize t h a t B t may work w e l l on h i g h - t a n n i n adapted p e s t s (with e l e v a t e d gut pH), such as those f e e d i n g on l a t e s u c c e s s i o n a l o r slow-growing t r e e s p e c i e s , but i t may be l e s s e f f e c t i v e on e a r l y s u c c e s s i o n a l species o r e a r l y i n the growth season on h i g h - t a n n i n t r e e s . NPV may be more e f f e c t i v e i n e a r l y s u c c e s s i o n a l s i t u a t i o n s o r any s i t u a t i o n where t a n n i n s are not important p l a n t defenses. I n a d d i t i o n , some p l a n t chemicals may make c e r t a i n b i o l o g i c a l c o n t r o l agents l e s s e f f e c t i v e . Examples i n c l u d e p l a n t chemicals which are t o x i c t o p a r a s i t o i d s (24) and those which are a n t i b a c t e r i a l (e.g., monoterpenes i n c o n f e r s ; 26). Knowledge o f n a t u r a l v a r i a t i o n i n p l a n t chemistry c o u l d g r e a t l y a i d i n improving such c o n t r o l methods. F i n a l l y , I would suggest t h a t p l a n t v a r i a b i l i t y , genotypic and/or phenotypic, i s as important t o t r e e s as i t i s t o herbaceous s p e c i e s such as crop p l a n t s . I t should thus be as important i n t r e e p l a n t a t i o n s and f o r e s t management as i t has become i n a g r i c u l t u r e . As f o r e s t management takes on more c h a r a c t e r i s t i c s o f l a r g e s c a l e a g r i c u l t u r e , perhaps we should take a l e s s o n from the mad scramble f o r o l d "new" genes i n corn and other crops and a v o i d the mistakes i n h e r e n t i n l a r g e , uniform p l a n t a t i o n s (11,75,76). Tree defense v a r i a b i l i t y may be as important or more important than uniform r e s i s t a n c e per se. I t seems reasonable t o suggest m a i n t a i n i n g i t o r mimicking i t under i n t e n s e management c o n d i t i o n s . C e r t a i n l y , there are s u b s t a n t i a l grounds f o r c o n c e n t r a t i n g r e s e a r c h e f f o r t s on s t u d i e s o f v a r i a n c e as w e l l as means. Acknowledgements Ideas were developed i n c o n v e r s a t i o n w i t h I.T. Baldwin, R.T. Holmes, and P.J. Nothnagle. I.T. Baldwin c a r r i e d out chemical analyses o f b i r c h and maple l e a v e s , and M.J. Richards drew the f i g u r e s . I thank M i c h a e l Montgomery, USDA F o r e s t S e r v i c e , f o r p e r m i s s i o n t o use unpublished data. Supported by NSF grant


52


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1982


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