Host Plant Resistance to Pests

12 Antifeedant Sesquiterpene Lactones in the Compositae

Downloaded by QUEENSLAND UNIV OF TECHNOLOGY on October 14, 2014 | http://pubs.acs.org Publication Date: June 1, 1977 | doi: 10.1021/bk-1977-0062.ch012

T O M J. MABRY and JAMES E. GILL Department of Botany, University of Texas, Austin, T X 78712 WILLIAM C. BURNETT, JR. and SAMUEL B. JONES, JR. Department of Botany, University of Georgia, Athens, GA 30602

Most of the known 700 or so sesquiterpene lactones are characteristic constituents of many members of the Compositae, occurring only infrequently in a few other higher and lower plants (1,2)· Whether or not the a , β-unsaturated γ-lactone function present in most of these terpenoids i s responsible f o r their antifeedant properties i s not known; however, this functionality has been implicated i n most of the other biological activities known f o r these substances: e.g. antitumor, cytotoxicity, contact dermatitis, and antifungal properties. Since we recently described i n detail the role of sesquiterpene lactones i n plant-animal interactions (2), the present account w i l l only summarize our specific findings concerning the way the germacranolide glaucolide-A (I) controls the level of feeding of insects and mammals on members of the genus Vernonia (3) and our general conclusions concerning the function of sesquiterpene lactones as antifeedants. In connection with establishing the antifeedant and growth inhibition properties of glaucolide-A (I), a germacranolide-type sesquiterpene lactone from Vernonia (Compositae), six species of Lepidoptera as well as two species of mammals were u t i l i z e d i n a series of laboratory and f i e l d tests with V. gigantea and V. glauca, both of which contain glaucolide-A, and with V. f l a c c i d i f o l i a , a species which does not produce any sesquiterpene lactones. Some of the major findings of these tests are summarized i n Table I and Figure 1. Insect Antifeedant Tests All of the six lepidopterous larvae used i n testing the feeding deterrent properties of glaucolide-A i n the laboratory tests are sympatric with the species of Vernonia tested and three of them, the yellowstriped armyworm, (Spodoptera ornithogalli), cabbage looper (Trichoplusia n i ) , and the yellow woollybear (Diacrisia virginica), feed i n nature on Vernonias containing glaucolide-A; a fourth species, the saddleback caterpillar

179

In Host Plant Resistance to Pests; Hedin, P.; ACS Symposium Series; American Chemical Society: Washington, DC, 1977.

HOST P L A N T RESISTANCE T O PESTS


180

( S i b i n e s t i m u l e a ) , feeds on V. f l a c c i d i f o l i a , a species l a c k i n g glaucolide-A. Two g e n e r a l i s t feeders, the f a l l and southern armyworms (Spodoptera e r i d a n i a and j>. f r u g i p e r d a ) , were not detected on Vernonias i n the f i e l d . The l a b o r a t o r y t e s t s e s t a b l i s h e d two trends (Table I ) : firstly, when the i n s e c t s had a choice of Vernonia f l a c c i d i f o l i a l e a f m a t e r i a l prepared i n the form of a p e l l e t with and without added g l a u c o l i d e - A , a l l the larvae p r e f e r r e d the d i e t without the sesquiterpene lactone; secondly, when the l a r v a e were o f f e r e d a choice of f r e s h leaves of g l a u c o l i d e - A species versus f r e s h leaves of V. f l a c c i d i f o l i a , they tended to e x h i b i t the same feeding patterns observed i n nature (4). That i s , except f o r the y e l l o w s t r i p e d armyworm, those species observed i n the f i e l d on Vernonias containing g l a u c o l i d e - A p r e f e r r e d these same p l a n t s over V. f l a c c i d i f o l i a i n the l a b o r a t o r y ; similarly, the one species observed on V. f l a c c i d i f o l i a under n a t u r a l conditions s t i l l p r e f e r r e d t h i s species i n the l a b o r a t o r y . Two g e n e r a l i s t feeders, the southern and f a l l armyworms, always avoided the g l a u c o l i d e - A p l a n t s . In t e s t s with the f a l l armyworm l a r v a e , i t was f u r t h e r determined that l e v e l s of about 1% g l a u c o l i d e - A ( i n a p e l l e t ) gave maximum deterrence; t h i s i s roughly the quantity of l a c t o n e m a t e r i a l synthesized i n the leaves of many sesquiterpene l a c t o n e - c o n t a i n i n g Compositaes.

Q

Glaucolide-A (Vernonia) (i)

L a r v a l Growth I n h i b i t i o n Tests Newly hatched larvae of the southern, fall, and y e l l o w s t r i p e d armyworms, cabbage looper, and yellow woollybear were reared on d i e t s c o n t a i n i n g g l a u c o l i d e - A i n amounts ranging up to 0.5%. The growth of the three armyworms was g r e a t l y reduced (Figure 1) and the r e d u c t i o n i n growth f o r the f a l l and southern armyworms was considerably greater than the decrease i n feeding. Moreover, except f o r the yellow woollybear, the


12.

MABRY ET A L .

Table I*

Antifeedant

Sesquiterpene

Lactones

181

Insect Antifeedant Tests

D i e t Preference i n Laboratory


Leaf Glaucolide-A Species

P e l l e t Choice

Choice V.

flaccidifolia

Insects:

V. f l a c . With Added Glauco lide-A

V. f l a c . Without Glauco lide-A

Observed on Glaucolide-A Vernonias 1. 2. 3.

Yellow Woollybear Cabbage Looper Yellowstriped Armyworm

χ (usually)

X

X

X X

X

X

*

X

X

X

X

Not Observed On Glaucolide-A Vernonias 1. 2. 3.

Saddleback Caterpiller Fall Armyworm Southern Armyworm

*Not t e s t e d ; c u l t u r e d i e d .



182

HOST P L A N T RESISTANCE

T O PESTS

Figure 1. Relative size of larvae reared on diets containing glaucolide-A. Top insect fed on control diet without added lactone; others were fed on diets containing 1/8%, 1/4%, and 1/2% ghucolide-A by dry weight. (A) Fall armyworm; (B) southern armyworm; (C) yellow-striped armyworm; (D) cabbage looper; (E) yellow woolybear.



12.

MABRY ET

AL.

Antifeedant

Sesquiterpene

Lactones

183

presence of g l a u c o l i d e - A i n the d i e t s increased the number of days to pupation f o r a l l species. Reduced survival was e s p e c i a l l y evident f o r the southern and f a l l armyworms during the e a r l y l a r v a l i n s t a r s (6). A l t o g e t h e r , the growth i n h i b i t i o n t e s t s demonstrated that glaucolide-A i s detrimental to c e r t a i n stages i n the l i f e c y c l e of s e v e r a l lepidopterous l a r v a e . In a separate s e r i e s of experiments, i t was a l s o e s t a b l i s h e d that except f o r the f a l l armyworm, the presence of g l a u c o l i d e - A on the leaves of Vernonias d i d not deter o v i p o s i t i o n by the species of Lepidoptera tested (7). Having e s t a b l i s h e d that g l a u c o l i d e - A could deter the feeding of some but not a l l i n s e c t larvae i n l a b o r a t o r y t e s t s , both t r a n s p l a n t garden and n a t u r a l f i e l d p l o t s of Vernonias were observed f o r the r e l a t i v e amounts of herbivory with respect to those p l a n t s which do and those p l a n t s which do not produce sesquiterpene lactones. S u r p r i s i n g l y , i n a l l cases, Vernonia f l a c c i d i f o l i a was fed upon l e s s than g l a u c o l i d e - A containing species, a result f o r which we do not yet have a s a t i s f a c t o r y explanation; however, we b e l i e v e that t h i s p u z z l i n g observation must be viewed i n l i g h t of the mammalian antifeedant experiments described below. Mammalian Antifeedant

Tests

At the outset, i t may be noted that cows avoided a l l Vernonias presumably on the b a s i s of having p r e v i o u s l y determined by t r i a l and e r r o r that most of these morphologically similar plants were b i t t e r (due to the presence of sesquiterpene lactones)· Eastern c o t t o n t a i l r a b b i t s and the w h i t e t a i l deer were both found to feed p r i m a r i l y on Vernonia f l a c c i d i f o l i a , not the g l a u c o l i d e - A species i n c o n t r o l l e d t e s t s . Moreover, both avoided the V. flaccidifolia a f t e r i t s leaves had been coated with glaucolide-A; i n this l a t t e r test, the deer would t a s t e the coated V. flaccidifolia, detect the b i t t e r compound, and then refuse to eat the p l a n t . I t was d i f f i c u l t to monitor mammalian feeding in the f i e l d s i n c e the g l a u c o l i d e - A species are apparently not eaten at a l l by mammals; i n c o n t r a s t , we assume on the b a s i s of our c o n t r o l l e d feeding experiments with deer and r a b b i t s that V. f l a c c i d i f o l i a i n the f i e l d would be totally consumed i f encountered. From the laboratory i n s e c t feeding t e s t s , i t i s evident that g l a u c o l i d e - A can deter the feeding and induce growth r e d u c t i o n of some but not a l l i n s e c t l a r v a e . Nevertheless, i n the f i e l d i t s absence from Vernonia f l a c c i d i f o l i a d i d not r e s u l t i n heavier feeding by i n s e c t s r e l a t i v e to V. gigantea and V. glauca (8). It i s of i n t e r e s t to note that the two species of Vernonia i n North America l a c k i n g sesquiterpene lactones, V. flaccidifolia and V. p u l c h e l l a , are a l s o species with r e s t r i c t e d ranges; we


184

HOST

suggest that mammalian feeding may account ranges and s m a l l p o p u l a t i o n s i z e s .

PLANT

RESISTANCE T O PESTS

f o r these

restricted


Summary In summary, g l a u c o l i d e - A apparently p r o t e c t s such species as Vernonia gigantea and V. glauca against a l l sympatric animals and some i n s e c t s . In c o n t r a s t , V. f l a c c i d i f o l i a has no chemical p r o t e c t i o n against mammals but nevertheless has evolved a s t i l l unknown but s a t i s f a c t o r y defense against insects. Most sesquiterpene lactones are b i t t e r suggesting that many members of t h i s c l a s s of n a t u r a l products serve as mammalian a n t i f e e d a n t s . Nevertheless, insect antifeedant p r o p e r t i e s must have been important i n the widespread s e l e c t i o n of sesquiterpene lactones i n the l a r g e s t of f l o w e r i n g p l a n t f a m i l i e s , the Compositae. Acknowledgement s Part of the research described here was supported by the N a t i o n a l Science Foundation (Grant DEB 76-09320 to T.J.M. ; GB-20687A and GB-39712 to S.B.J.), N a t i o n a l I n s t i t u t e s of Health (Grant HDO 04488 t o T.J.M.), and the Robert A. Welch Foundation (Grant F-130 to T.J.M.). Literature Cited

1. Yoshioka, H., Mabry, T. J., and Timmermann, Β. Ν., "Sesquiterpene Lactones", Univ. of Tokyo Press, Tokyo, 1973. 2. Burnett, W. C., Jr., Mabry, T. J. and Jones, S. B., Jr., "The Role of Sesquiterpene Lactones in Plant-Animal Coevolution", in "Biochemistry of Plant-Animal Coevolution", J. B. Harborne, ed., Academic Press, London, (in press). 3. Burnett, W. C., Jr., "Sesquiterpene Lactones -- Herbivore Feeding Deterrents in Vernonia (Compositae)". Ph. D. Dissertation, University of Georgia, Athens, 1974. 4. Burnett, W. C., Jr., Jones, S. B., Jr., Mabry, T. J., and Padolina, W. G., Biochem. Syst. Ecol., (1974), 2:25-29 . 5. Burnett, W. C., Jr., Jones, S. B., Jr., and Mabry, T. J., Taxon (in press), (1977a). 6. Burnett, W. C., Jr., Jones, S. B., Jr., and Mabry, T. J., Amer. Midl. Natur. (in press), (1977b). 7. Burnett, W. C., Jr., Jones, S. B., Jr., Mabry, T. J., and Betkouski, M. F., Oecologia (submitted), (1977c). 8. Burnett, W. C., Jr., Jones, S. B., Jr., and Mabry, T. J., Plant Syst. Evol. (submitted), (1977d).


Host Plant Resistance to Pests

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