Physiological Constraints on Plant Chemical ... - ACS Publications

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Downloaded by UNIV OF CALIFORNIA SANTA BARBARA on June 15, 2016 | http://pubs.acs.org Publication Date: January 20, 1983 | doi: 10.1021/bk-1983-0208.ch002

Physiological Constraints on Plant Chemical Defenses H . A . M O O N E Y , S. L. G U L M O N , and N. D . J O H N S O N Stanford University, Department of Biological Sciences, Stanford, C A 94305

Plants allocate their carbon and nitrogen resources to a variety of functions including constructing and maintaining new tissues (root, shoot, reproductive), storage, and defense from herbivores. There i s a genetically-determined time schedule of allocation of resources to various functions which can be modified to a certain degree by environmental conditions. The proposition i s examined that this time schedule represents changing allocation p r i o r i t i e s within the plant which results i n time "windows" when i t is more susceptible to herbivore damage than others. Anti-herbivore "strategies" of plants must be considered i n r e l a t i o n to changing patterns of resource a v a i l a b i l i t y to the whole plant and i n r e l a t i o n to allocation of these resources to enhance reproductive output. P l a n t - i n s e c t i n t e r a c t i o n has been considered e x t e n s i v e l y from the view p o i n t of the chemistry involved i n p l a n t defense ( f o r example reviews i n I), the growth c y c l e of the plant as i t a f f e c t s i t s "apparency" t o herbivores (2_), and the seasonal p h y s i c a l and b i o t i c environment of the herbivores ( 3 ) . Here we consider the i n t e r a c t i o n of the p l a n t ' s p h y s i c a l environment, that i s , i t s changing resource a v a i l a b i l i t y p a t t e r n , w i t h the u t i l i z a t i o n of these resources f o r growth, reproduction and defense against herbivores.The production of p l a n t defensive chemicals i s , o p t i m a l l y , governed by the cost of the chemicals, t h e i r e f f e c t i v e n e s s a t d e t e r r i n g h e r b i v o r y , the r i s k o f h e r b i v o r y , and the cost of herbivory. The e f f e c t i v e n e s s of d i f f e r e n t chemicals a t d e t e r r i n g h e r b i v o r y has been e x t e n s i v e l y s t u d i e d , and t h e o r i e s concerning the r i s k of herbivory are w e l l e s t a b l i s h e d . Much l e s s I s known about the costs of h e r b i v o r y or the costs of defensive chemicals. The costs of defensive 0097-6156/83/0208-0021$06.00/0 © 1983 American Chemical Society

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

PLANT RESISTANCE TO INSECTS


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chemicals are a f u n c t i o n of t h e i r b i o s y n t h e t i c maintenance and turnover c o s t s , but a l s o a f u n c t i o n of the value of the elements used i n t h e i r c o n s t r u c t i o n . The value of these resources w i l l be determined by t h e i r importance to other a c t i v i t i e s such as reproduction, photosynthesis, n u t r i e n t uptake, or support. Here we assess the consequences, i n terms of herbivore s u s c e p t i b i l i t y , of simultaneous uses of l i m i t i n g resources by p l a n t s f o r a v a r i e t y of necessary f u n c t i o n s . We e a r l i e r discussed c o s t s of defensive compounds i n r e l a t i o n to h e r b i v o r y (_4). Carbon and n i t r o g e n are the two primary resources which can be a l l o c a t e d to defensive s t r u c t u r e s and which may a l s o be l i m i t i n g i n a p l a n t . They are used d i r e c t l y i n the c o n s t r u c t i o n of secondary compounds or p r o t e c t i v e s t r u c t u r e s , and carbon i s a l s o used as an energy source to c o n s t r u c t these components. The supply of f i x e d carbon i s an i n t e g r a t i o n of the a v a i l a b i l i t y of a l l the resources l i m i t i n g photosynthesis i n c l u d i n g l i g h t , water, and n u t r i e n t s . Temperature a c t s i n d i r e c t l y to c o n t r o l resource a v a i l a b i l i t y . V a r i a t i o n i n any of these r e s u l t s i n f l u c t u a t i o n s i n carbon g a i n and r e c u r r e n t c y c l e s of storage and u t i l i z a t i o n of carbon i n d i f f e r e n t p a r t s of the plant ( F i g . 1). L i m i t a t i o n s on the supply of n i t r o g e n and carbon could r e s u l t i n " p r i o r i t i e s " of use w i t h i n the p l a n t i n order to maximize f i t n e s s . In the f i r s t part of t h i s paper we consider general aspects of both n i t r o g e n and carbon a l l o c a t i o n . Then we examine the way carbon a l l o c a t i o n p r i o r i t i e s a f f e c t defense from herbivores i n a p a r t i c u l a r v e g e t a t i o n type, the temperate deciduous f o r e s t . Nitrogen N i t r o g e n i s a component of s e v e r a l c l a s s e s of compounds b e l i e v e d to be important i n p l a n t chemical defense, p r i n c i p a l l y cyanogenic g l y c o s i d e s , g l u c o s i n o l a t e s , a l k a l o i d s , c e r t a i n p r o t e i n s , and non-protein amino a c i d s and peptides. The n i t r o g e n c o n c e n t r a t i o n i n leaves i s o f t e n l i m i t i n g to i n s e c t l a r v a l growth (see review by Mattson, _5), and i t i s a primary l i m i t i n g f a c t o r to l e a f carbon-gaining c a p a c i t y (6^ 7_ 8). A l l o c a t i o n of n i t r o g e n to chemical defense must be considered w i t h i n the context of t h i s complex interdependency. The q u a n t i t a t i v e commitment of n i t r o g e n to secondary compounds v a r i e s c o n s i d e r a b l y . At one extreme, the n i c o t i n e c o n c e n t r a t i o n of tobacco leaves ( N l c o t l a n a tabacum) can range from 0.17 to 4.93% ( 9 ) . At the upper l e v e l , t h i s i s equivalent to n e a r l y 1% l e a f n i t r o g e n c o n c e n t r a t i o n , s i n c e n i c o t i n e i s over 17% n i t r o g e n by weight. The t o t a l n i t r o g e n c o n c e n t r a t i o n i n leaves r a r e l y exceeds 5%, so n i c o t i n e may comprise up to 20% of the n i t r o g e n In the l e a f . Not s u p r i s i n g l y , n i c o t i n e production i s c o r r e l a t e d w i t h f e r t i l i z e r a p p l i c a t i o n ( 9 ) . In another example, the cyanogenic g l u c o s i d e content i n the 9



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Resource availability Uptake Allocation

Stores Retrieval

Growth

Protection

Leaf Support Root Reproduction

I

t Loss Figure 1.

Flow scheme for a resource within a plant.


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leaves of the evergreen c h a p a r r a l shrub Heteromeles a r b u t i f o l i a a t t a i n s 7% of t o t a l dry weight (10). Assuming, as the authors d i d , that a l l of the g l u c o s i d e was prunasin, t h i s i s equivalent to 0.33% n i t r o g e n by dry weight, or about o n e - t h i r d of the average t o t a l n i t r o g e n i n the l e a f ( 1 1 ) . On the other hand, most a l k a l o i d s c o n t a i n much l e s s n i t r o g e n as a f r a c t i o n of the t o t a l weight than n i c o t i n e (Table I ) , and t o x i c compounds such as a l k a l o i d s are u s u a l l y found a t very low concentrations i n the p l a n t (12). Thus, the a l l o c a t i o n of n i t r o g e n t o nitrogenous secondary compounds can range from s u b s t a n t i a l t o n e g l i g i b l e , even w i t h comparable a l l o c a t i o n s of carbon. Another f a c t o r which i s important i n c o n s i d e r i n g the commitment of n i t r o g e n to chemical defense i s the high m o b i l i t y of t h i s element w i t h i n the p l a n t . In f o r e s t v e g e t a t i o n , 20-40% of the n i t r o g e n i n senescing leaves I s resorbed (13). Nitrogen i s r e a d i l y moved from senescing leaves to developing f r u i t s (14), and i n deciduous trees a s u b s t a n t i a l part of s p r i n g growth i s made u s i n g n i t r o g e n stored i n the r o o t s and stem wood and bark (15, 16). The n i t r o g e n i n secondary compounds a l s o appears to be r e a d i l y mobile and metabolizable. When doubly-labeled n i c o t i n e ( C N) was f e d to tobacco (]¥. r u s t i c a ) , carbon was recovered i n a l k a l o i d s , f r e e amino a c i d s , pigments, f r e e organic acids and f r e e sugars; and n i t r o g e n was recovered i n p r o t e i n s , a l k a l o i d s , f r e e amino a c i d s and pigments ( 1 7 ) . C e r t a i n n i t r o g e n - c o n t a i n i n g t o x i c compounds found i n seeds are completely degraded during germination (18). Other examples o f a l k a l o i d turnover are given i n Robinson (19) and Digenis ( 2 0 ) . Examples of t r a n s l o c a t i o n of n i t r o g e n - c o n t a i n i n g secondary compounds i n c l u d e the cyanogenic g l u c o s i d e , l i n a m a r i n , i n the w i l d lima bean (Phaseolus l u n a t u s ) , which i s t r a n s l o c a t e d from seeds to developing seedlings (21). R i c i n i n e i n c a s t o r beans i s t r a n s l o c a t e d from senescent leaves t o young, developing t i s s u e and t o seeds. Caffeine i s a l s o t r a n s l o c a t e d among leaves and i n t o f r u i t s (22). I n the case of Heteromeles a r b u t i f o l i a , c i t e d e a r l i e r , cyanogenic glucosides appear t o move from leaves i n t o developing seeds'. McKey (23) gives other examples of t r a n s l o c a t i o n of t o x i c compounds w i t h i n the p l a n t . Thus n i t r o g e n i n v e s t e d i n chemical defenses can be moved throughout the p l a n t to p r o t e c t v u l n e r a b l e organs such as young leaves or f r u i t s , and can l a t e r be reused f o r growth and development. Because nitrogenous compounds are r e a d i l y metabolized or transported w i t h i n the p l a n t , i t would seem that the major c o n s t r a i n t on use of n i t r o g e n i n chemical defense i s i t s e f f e c t i v e n e s s and the p a t t e r n of i t s a v a i l a b i l i t y i n the h a b i t a t . I f n i t r o g e n i s the major f a c t o r l i m i t i n g to growth, i t i s u n l i k e l y that l a r g e amounts w i l l be d i v e r t e d to secondary


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Table 1. Approximate percentages of n i t r o g e n i n some common plant a l k a l o i d s

Alkaloids caffeine nicotine ricinine gramine lupinine quinine mescaline colchicine tomatine

28.9 17.3 17.0 16.1 8.3 7.4 6.6 3.5 1 4

Toxic amino a c i d s 3amlno p r o p i o n i t r i l e canavanine mimosine Transport

40.0 31.8 14.1

amides asparagine glutamine

21.2 19.2

glycine alanine serine proline tyrosine

18.7 15.7 13.3 12.2 7.7

Amino a c i d s

Cyanogenic g l u c o s i d e s linamarin prunasin amygdalin

5.7 4.7 3.1



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compounds, e s p e c i a l l y s i n c e there are many non-nitrogenous plant products, such as c a r d i a c g l y c o s i d e s , saponins, f l a v o n o i d s , quinones, e t c , which are a l s o t o x i c . Although n i t r o g e n i s probably l i m i t i n g to some extent i n most n a t u r a l systems, i t i s not the major l i m i t i n g n u t r i e n t i n a l l of them, and i s not l i m i t i n g to the same extent a t a l l times of the year. In l a r g e areas of A u s t r a l i a f o r example, phosphorus i s the p r i n c i p l e l i m i t i n g element (24). Some p l a n t s experience a s h o r t - l i v e d abundance of n i t r o g e n . Most annuals occupy d i s t u r b e d or semi-disturbed h a b i t a t s which are c h a r a c t e r i z e d by a sudden r e l e a s e of n u t r i e n t s (25). Even many herbaceous p e r e n n i a l s occur under semi-disturbed c o n d i t i o n s (eg. o l d f i e l d s ) , or grow during a short i n t e r v a l between c l i m a t i c l i m i t a t i o n s and b i o t i c competition when resources are r e l a t i v e l y abundant, as i s the case of the f o r e s t understory f l o r a (26, 2 7 ) . P l a n t t o x i n s are widely d i s t r i b u t e d i n herbaceous s p e c i e s , as opposed to protein-complexing polyphenols which are more l i m i t e d to leaves of woody p e r e n n i a l s (12, 23). This p a t t e r n has been suggested t o r e l a t e to the low p r e d i c t a b i l i t y i n space and time of herbaceous f o l i a g e i n c o n t r a s t to the f o l i a g e of woody p l a n t s (2_, 12). However, i t should be noted t h a t , a t l e a s t i n the case of some annuals (9_, 28), a l l of the n i t r o g e n i s taken up during the p e r i o d of v e g e t a t i v e growth and simply r e d i s t r i b u t e d d u r i n g r e p r o d u c t i o n (Figure 2 ) . Although data are scarce, t h i s p a t t e r n may be widespread among herbaceous species s i n c e , as already s t a t e d , they o f t e n grow during a short p e r i o d of resource a v a i l a b i l i t y . Given a p a t t e r n of i n i t i a l r a p i d n u t r i e n t uptake and temporal storage i n some cases to high c o n c e n t r a t i o n s , i t i s c l e a r l y advantageous to maintain any n i t r o g e n not being used f o r photosynthesis or growth i n a form that i s t o x i c t o h e r b i v o r e s . Thus, the common occurrence of t o x i c nitrogenous compounds i n herbaceous p l a n t s may simply r e f l e c t resource a v a i l a b i l i t y p a t t e r n s and consequent a l l o c a t i o n pathways. This p a t t e r n may a l s o apply to some woody p e r e n n i a l s . For example, c h a p a r r a l shrubs have periods of a c t i v e n i t r o g e n uptake i n the f a l l when growth i s not o c c u r r i n g (29). This s t o r e d n i t r o g e n i s moved to new growth i n the s p r i n g and a p o r t i o n i s a l l o c a t e d to nitrogenous defensive compounds (10). Carbon L i k e n i t r o g e n a c q u i s i t i o n , the carbon-gaining c a p a c i t y of a plant i s environmentally l i m i t e d . As described e a r l i e r , t h i s l i m i t a t i o n r e s u l t s i n apparent " p r i o r i t i e s " f o r a l l o c a t i o n t o storage, growth of d i f f e r e n t organs, and e l a b o r a t i o n of v a r i o u s c l a s s e s of m e t a b o l i t e s . These a l l o c a t i o n patterns change during the seasonal growth of an i n d i v i d u a l . I n t r e e s , f o r example, root growth g e n e r a l l y takes place a t times d i f f e r e n t



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from stem e l o n g a t i o n which i n t u r n i s d i s p l a c e d from stem diameter growth (30, 31) (Figure 3 ) . Carbon metabolism d i f f e r s fundamentally from n i t r o g e n metabolism i n that v i r t u a l l y a l l nitrogenous compounds can be r e c y c l e d w i t h i n the p l a n t , whereas most of the s t r u c t u r a l components of the p l a n t , p r i n c i p a l l y c e l l u l o s e and l i g n i n , a r e not reusable. There are a l s o p u t a t i v e defensive compounds i n t h i s category such as l e a f - e x t e r n a l r e s i n s (32) and p o s s i b l y some condensed t a n n i n s . Thus the c o n s t r a i n t s on a l l o c a t i o n have both an immediate and f u t u r e time frame. The i n t e r a c t i o n s between a v a i l a b i l i t y of resources, carbon g a i n i n g c a p a c i t y , and the a l l o c a t i o n of carbon t o p l a n t f u n c t i o n s , i n c l u d i n g chemical defense, w i l l o b v i o u s l y d i f f e r among environments. We examine a p a r t i c u l a r system, t h e temperate deciduous f o r e s t , t o i l l u s t r a t e the nature of the c o n s t r a i n t s on chemical defenses imposed by l i m i t a t i o n s on carbon gain. The Deciduous Forest In s p r i n g , 80% of the deciduous f o r e s t canopy i s produced over a short span of time (31, 33, 34) (Figure 3). I n i t i a l l e a f expansion, f l o w e r i n g and shoot e x t e n s i o n are h e a v i l y s u b s i d i z e d from carbohydrate reserves because there i s i n s u f f i c i e n t p h o t o s y n t h e t i c area t o support these processes (35, 36) ( F i g . 4 ) . Despite the demand on carbohydrate s t o r e s , reserves are not completely depleted and appear t o be renewed r a p i d l y f o l l o w i n g the growth f l u s h e s (16). I t has been suggested that maintenance of some storage i s important i n the event the f i r s t l e a f crop i s destroyed due t o i n t e n s e h e r b i v o r y (37) o r a l a t e k i l l i n g f r o s t (31), and a second crop must be produced. Deciduous t r e e s vary i n the d u r a t i o n of l e a f i n i t i a t i o n and expansion and new shoot e x t e n s i o n (38-41). This v a r i a t i o n i s t y p i f i e d by two type examples ( F i g u r e 5): Quercus s p e c i e s complete a l l l e a f and shoot growth during a s h o r t p e r i o d , u s u a l l y l a t e A p r i l t o e a r l y June; B e t u l a , by c o n t r a s t , grows throughout most o f the summer. Fagus, Carya, and Fraxinus have growth c y c l e s of the Quercus type, and L l r l o d e n d r o n , Populus, and Llquldamber have extended growth c y c l e s l i k e B e t u l a . Acer species are i n t e r m e d i a t e . The r e l a t i o n s h i p between d u r a t i o n of stem e l o n g a t i o n and dependence on carbohydrate reserves needs to be e s t a b l i s h e d f o r these t r e e s , o b v i o u s l y though oak species which form canopies e n t i r e l y from pre-formed l e a f buds have a heavy d r a i n on carbon reserves f o r a p e r i o d . The young leaves c o n s t i t u t e an abundant food resource f o r phytophagous i n s e c t s and they are e s p e c i a l l y v u l n e r a b l e t o h e r b i v o r e s due to a h i g h n i t r o g e n content and l a c k o f s c l e r o p h y l l y . These c h a r a c t e r i s t i c s appear t o be u n i v e r s a l i n new leaves of deciduous f o r e s t s p e c i e s , and t h i s p e r i o d o f



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Figure 3. Seasonal growth activity of a white oak in Missouri. Development of canopy photosynthetic capacity is shown in A. Relative seasonal growth activity of various tree components are given in B. Key: F, flower; S, shoot; L, leaf; SC, stem circumference; RG, root growth; and A, acorn. (Reproduced with permission from Ref.31.)



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4 2 -

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Months Figure 4. Seasonal changes in available carbohydrates in a Californian evergreen oak (A), a Vermont sugar maple (B), and a Calif ornian buckeye (C). Maple data for sapwood are from Ref. 15. Oak and buckeye data are from Ref. 49, for total branch minus fruits. The evergreen oak has a stable supply of carbon through continuous photosynthesis. The maple draws upon reserves in the spring to build a new canopy. The buckeye draws upon reserves to build fruits in the fall as well as new canopy in late January.



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20 30 10 April May Figure 5.

Seasonal height growth of three deciduous species (39). Key: O, white ash; - • red maple; and gray birch.



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v u l n e r a b i l i t y t y p i c a l l y l a s t s about one month (42, 43, 44) (Figure 6 ) . Apparently, the p o t e n t i a l f o r reducing t h i s window of v u l n e r a b i l i t y i s f a i r l y l i m i t e d . The p r o t e i n content o f developing leaves could conceivably be reduced but t h i s would slow the metabolic processes o f growth and reduce the gross photosynthetic rate- Both would r e s u l t i n longer development times, prolonging v u l n e r a b i l i t y , and be a heavier d r a i n on r e s e r v e s , consequences which would reduce a t r e e ' s competitive advantage. A somewhat s i m i l a r c o n s t r a i n t a p p l i e s t o the e a r l y development of s c l e r o p h y l l y , a p o t e n t i a l h e r b i v o r e d e t e r r i n g f e a t u r e . C o n s t r u c t i o n of r i g i d c e l l w a l l s and the production of l i g n i n and other compounds would c e r t a i n l y slow the o v e r a l l r a t e of l e a f expansion and prolong the p e r i o d during which the l e a f i s a net importer of carbon r e s e r v e s . We have already mentioned that r a p i d canopy development i s an important competitive advantage and minimizes the time d u r i n g which young leaves are v u l n e r a b l e to h e r b i v o r e s . Climate can sometimes be an a d d i t i o n a l c o n s t r a i n t . For example, i n the white oak f o r e s t i n M i s s o u r i , l e a f development occurs during an i n t e r v a l o f optimal growing c o n d i t i o n s between the l a t e s t k i l l i n g f r o s t and the midsummer drought (31). Deployment o f defensive chemicals during l e a f

expansion.

Toxins appear t o be e f f e c t i v e i n s m a l l q u a n t i t i e s (12), making them an i d e a l low cost defense against g e n e r a l i s t herbivores even though s p e c i a l i s t s are able t o evolve e f f e c t i v e d e t o x i f i c a t i o n mechanisms. Studies have shown t h a t t o x i n c o n c e n t r a t i o n s are g e n e r a l l y higher i n new growth (23, 45), but there have been few s t u d i e s o f temperate deciduous t r e e s . I t has been shown that g e n e r a l i s t herbivores are more common on mature f o l i a g e whereas s p e c i a l i s t h e r b i v o r e s p r e f e r new f o l i a g e (46), but again, there are few s t u d i e s i n the temperate deciduous f o r e s t . Protein-complexing polyphenols are broadly e f f e c t i v e against h e r b i v o r e s , e s p e c i a l l y those not s p e c i f i c a l l y adapted to eat p l a n t s c o n t a i n i n g polyphenols (47). They may c o n s t i t u t e 10% o r more o f the l e a f dry weight (12, 37, 44), and t h i s r e q u i r e s a l l o c a t i o n of s i g n i f i c a n t amounts of carbon and energy to t h e i r c o n s t r u c t i o n . The use of l i m i t e d reserves f o r such q u a n t i t a t i v e defenses must be balanced a g a i n s t the requirements of r a p i d canopy development and new shoot e x t e n s i o n . P a t t e r n s of polyphenol accumulation i n leaves vary among the few temperate f o r e s t species which have been s t u d i e d . Feeny s (42) c l a s s i c study on oak leaves (Quercus robur) shows l e a f t a n n i n l e v e l s r i s i n g s l o w l y u n t i l August, and then i n c r e a s i n g s h a r p l y . In the cases of sugar maple (Acer saccharum) and y e l l o w b i r c h ( B e t u l a l u t e a ) (44), r e s p e c t i v e l y , 1



Figure 6. Seasonal changes in leaf nitrogen (A) and leaf toughness (B) of a series of deciduous tree species. (Reproduced with permission from Ref. 43.)



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33

polyphenol concentrations peak i n l a t e June and mid May. In Betula pubescens (48) the c o n c e n t r a t i o n o f tannins i s s t a b l e u n t i l l a t e summer and then Increases. Feeny (2) has coined the term "apparency" t o express t h e i d e a that some p l a n t s o r p l a n t components are more p r e d i c t a b l e resources i n space and time t o p o t e n t i a l h e r b i v o r e s . He suggests that such p r e d i c t a b l e p l a n t s are more a t t r a c t i v e t o s p e c i a l i s t herbivores ( i n e v o l u t i o n a r y time) because o f t h e i r p r e d i c t a b i l i t y , and thus should employ q u a n t i t a t i v e defensive compounds which are l e s s s u s c e p t i b l e t o the e v o l u t i o n o f d e t o x i f i c a t i o n mechanisms. We propose that the p a t t e r n s of polyphenol production i n leaves are r e l a t e d t o the d u r a t i o n of new l e a f p r o d u c t i o n . Species which accomplish l e a f expansion and shoot extension w i t h i n a short time p e r i o d , e s p e c i a l l y i n c o l d c l i m a t e s , should g e n e r a l l y have low polyphenol concentrations i n young leaves compared t o species w i t h extended periods of a c t i v e growth. There are two reasons f o r the above. F i r s t , the new leaves of species w i t h short growth periods a r e l e s s "apparent" i n the sense Feeny (2) has described. They appear e a r l y , when predator populations may be i n h i b i t e d by c o l d temperatures, and are not present long enough t o a l l o w build-up of predator p o p u l a t i o n s . By c o n t r a s t , new leaves o f species w i t h long growth periods are present over an extended p e r i o d of time, g e n e r a l l y much o f the summer, and thus c o n s t i t u t e a p r e d i c t a b l e resource f o r s p e c i a l i z e d h e r b i v o r e s . Second, new l e a f and shoot growth are a g r e a t e r d r a i n on p l a n t reserves when the e n t i r e canopy i s produced over a short time p e r i o d (35). In such s p e c i e s , a l l o c a t i o n of 10-25% o f new l e a f dry weight t o polyphenol p r o d u c t i o n would f u r t h e r deplete reserves, slow canopy development, o r both. This would decrease the advantage that such species have i n terms of escaping h e r b i v o r y i n time, and would a l s o reduce the p e r i o d o f carbon g a i n which determines reserves and p o t e n t i a l growth f o r the f o l l o w i n g season. The p a t t e r n s o f polyphenol accumulation i n Quercus (42) and Acer and B e t u l a (44) are c o n s i s t e n t w i t h t h i s hypothesis, but examination of polyphenol concentrations through time i n many more species i s necessary. Schultz et a l . (44) suggest t h a t the low polyphenol contents of young leaves may be due t o the f a c t that p r o t e i n s y n t h e s i s suppresses phenolic synthesis. To summarize, s p e c i f i c t o x i n s are e f f e c t i v e d e t e r r e n t s t o g e n e r a l i s t h e r b i v o r e s , but polyphenols produced i n r e l a t i v e l y l a r g e q u a n t i t i e s are the only e f f e c t i v e d e t e r r e n t t o s p e c i a l i s t s . Since l e a f toughness and lower n i t r o g e n content a l s o deter many h e r b i v o r e s , deciduous f o r e s t t r e e s are e s p e c i a l l y v u l n e r a b l e t o a t t a c k during the p e r i o d o f canopy development, which occurs y e a r l y a t a p r e d i c t a b l e time. Canopy development i s h e a v i l y dependent on a v a i l a b l e reserves o f carbohydrate and n i t r o g e n , and the production o f q u a n t i t a t i v e


34



defensive compounds i s expensive i n terms of carbon and energy. I t t h e r e f o r e appears that the patterns of production of polyphenols during canopy development are r e l a t e d to the d u r a t i o n of new growth. Species which produce the e n t i r e canopy during the s h o r t e s t p e r i o d of time, thus i n c u r r i n g the greatest d r a i n on r e s e r v e s , may defer maximum polyphenol production u n t i l a f t e r the canopy i s mature. More i n f o r m a t i o n i s needed to examine these ideas. Summary In order to g a i n an understanding of the options which p l a n t s can u t i l i z e to defend themselves against herbivores we need a more comprehensive view of the carbon and n i t r o g e n a c q u i s i t i o n and a l l o c a t i o n p a t t e r n of p l a n t s of d i v e r s e h a b i t a t s . For example, there are c l e a r d i f f e r e n c e s i n the a l l o c a t i o n p a t t e r n s between annual versus p e r e n n i a l p l a n t s which r e l a t e to the resources a v a i l a b l e to them through time. Further, there are d i f f e r e n c e s i n the r e u t i l i z a t i o n p o s s i b i l i t i e s of e i t h e r carbon or n i t r o g e n compounds w i t h i n a plant as i t develops. These d i v e r s e a c q u i s i t i o n and a l l o c a t i o n p a t t e r n s place c o n s t r a i n t s on the p o s s i b l e defensive s t r a t e g i e s of p l a n t s and hence on the o p p o r t u n i t i e s f o r h e r b i v o r e a t t a c k . Acknowledgements. This paper grew out of work supported by NSF grant DEB810279. We thank B. L i l l e y f o r a s s i s t a n c e and F.S. Chapin I I I , J.C. S c h u l t z , G. P u t t i c k and J . Glyphis f o r comments on a v e r s i o n of t h i s paper.

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1982


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