Allelopathy in Desert Ecosystems - ACS Symposium Series (ACS

Chapter 6

Allelopathy in Desert Ecosystems

Downloaded by UNIV OF CALIFORNIA SAN DIEGO on March 4, 2016 | http://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch006

Jacob Friedman Department of Botany, George S. Wise Faculty of Life Sciences, Tel Aviv University, 69978, Israel

Allelopathy and autotoxicity in desert ecosystems in both hemispheres are reviewed. The following generalizations are made : (a) aggressive plants with allelopathic potential are often adult perennials, members of the Compositae or Labiatae, that are capable of reducing germination and/or growth of various annuals or of their own seedlings; (b) allelochemicals emanated from aggressive plants are either common secondary metabolites (terpenes, terpenoids, or phenolic compounds), or inorganic salts. Allelochemicals, although frequently nonspecific, do not constitute general phytocides. They may reach susceptible plants through the soil in different ways, either washed off from the fresh or dried shoots by rainfall, released as volatile substances later absorbed by the s o i l , or released in part from the mature or decomposed roots; (c) some ecological factors in the desert favor production of allelochemicals, e.g. water or mineral stresses, or grazing, whereas other factors improve the preservation of the allelochemicals, i . e . low rates of leaching, or reduced activity of the soil microflora. Wide desert areas are covered with sandy soils containing small amounts of organic material and this may account for a slow release of allelochemicals. Dependent upon such interactions, allelopathy may be manifested in a certain area and not at a l l in a similar one despite the presence of very similar plant populations in both areas. It is likely that further observations in desert areas that show a gradient of aridity will allow exploration of additional allelopathic effects.

0097-6156/87/0330-0053$06.00/0 © 1987 A m e r i c a n C h e m i c a l Society

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.


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ALLELOCHEMICALS: ROLE IN AGRICULTURE A N D FORESTRY

The s p a r s e v e g e t a t i o n i n a r i d environments p r o v i d e s an e x c e l l e n t model f o r s t u d y i n g g e r m i n a t i o n , p r o g r e s s i v e growth, and m o r t a l i t y o f i n d i v i d u a l p l a n t s . No wonder, t h e n , t h a t p i o n e e r i n g work on a l l e l o p a t h y was p e r f o r m e d i n v a r i o u s d e s e r t s of the w o r l d , and some o f t h i s work w i l l be d e s c r i b e d h e r e i n . F i r s t , however, I raise the c o n j e c t u r e t h a t a r i d c o n d i t i o n s may f a v o r p l a n t s p e c i e s endowed w i t h a l l e l o c h e m i c a l p o t e n t i a l , and t h i s more o f t e n than c u r r e n t l y r e a l i z e d . I b e l i e v e the a l l e l o c h e m i c a l e f f e c t i n t e r a c t s w i t h o t h e r e n v i r o n m e n t a l f a c t o r s and i s d i m i n i s h e d o r enhanced i n a c c o r d a n c e w i t h l o c a l changes i n the a r i d i t y . Because of the s p a t i a l and t e m p o r a l dependence of p l a n t i n t e r a c t i o n s , i n c o n s i s t e n c i e s i n the o b s e r v a t i o n s made a t d i f f e r e n t l o c a l i t i e s a r e i n e v i t a b l e , and f o r t h o s e who s t r u g g l e t o p r o v e a l l e l o p a t h y an element of u n c e r t a i n t y i s t h u s i n t r o d u c e d . I t i s t o be hoped t h a t an e x a c t i n g c o m b i n a t i o n o f e c o l o g i c a l o b s e r v a t i o n s w i t h b i o c h e m i c a l p r o c e d u r e s w i l l e n a b l e the t r a c i n g o f pathways t a k e n by p h y t o t o x i n s from the p r o d u c e r p l a n t t o the s u s c e p t i b l e one, and w i l l e v e n t u a l l y a l l o w a q u a n t i f i c a t i o n o f the a l l e l o p a t h i c e f f e c t . The purpose o f the p r e s e n t p a p e r i s t o r e v i e w some o f the work on a l l e l o p a t h y b e i n g u n d e r t a k e n i n v a r i o u s d e s e r t ecosystems i n the w o r l d , t o p o i n t out f a c t o r s t h a t may modify the e f f e c t of a g g r e s s i v e p l a n t s o r the response o f s u s c e p t i b l e ones, and t o e l a b o r a t e on the methodology employed t o a s s e s s a l l e l o p a t h y or a u t o t o x i c i t y . A l l e l o p a t h y i n D e s e r t s o f the Western Hemisphere The b e s t documentation o f p l a n t a l l e l o p a t h y d e r i v e s from the U n i t e d S t a t e s . For i n s t a n c e , i n the Borego V a l l e y of the Mojave D e s e r t , where the a n n u a l r a i n f a l l i s 200-255 mm, Went (1) n o t e d t h a t o n l y a few a n n u a l s were a s s o c i a t e d w i t h l i v i n g shrubs of E n c e l i a farinosa ( C o m p o s i t a e ) , whereas the d e n s i t y of a n n u a l s i n the v i c i n i t y o f dead E n c e l i a s h r u b s , as w e l l as near l i v i n g shrubs o t h e r than E n c e l i a , was much h i g h e r . Annuals n o t a s s o c i a t e d w i t h l i v i n g E n c e l i a were : Malacothrix californica, Emmenanthe p e d u l i f l o r a , Rafinesquia neomexicana ,and H i l a r i a r i g i d a . I t was f i r s t supposed t h a t t o x i c i t y i s i n d u c e d by the r o o t s o f E n c e l i a , but Gray and Bonner (2) were u n a b l e t o show any i n h i b i t i o n by such r o o t s , whereas e i t h e r f r e s h o r d r i e d l e a v e s o f E n c e l i a , when added t o sand-grown c u l t u r e s of tomato, i n h i b i t e d growth o f the s e e d l i n g s . Aqueous e x t r a c t o f E n c e l i a l e a v e s (0.025% on d r y weight b a s i s ) was e x t r e m e l y t o x i c t o c o r n and pepper, b u t b a r l e y , o a t s and s u n f l o w e r were o n l y s l i g h t l y a f f e c t e d . The p h y t o t o x i c p r i n c i p l e , c o l o r l e s s n e e d l e s w i t h a p l e a s a n t odor, was c r y s t a l l i z e d f r o m e x t r a c t s o f p l a n t s growing w i l d i n the C o l o r a d o D e s e r t , C a l i f o r n i a and i d e n t i f i e d as 3 - a c e t y l - 6 methoxybenzaldehyde ( F i g u r e 1) ( 3 ) . At a c o n c e n t r a t i o n of 1.4 mM, t h i s compound k i l l e d , w i t h i n 24 h, 100% o f tomato s e e d l i n g s grown i n sand c u l t u r e s . When t e s t p l a n t s were grown i n f e r t i l e garden s o i l , the e f f e c t was s m a l l e r , but Gray and Bonner have p o i n t e d out t h a t , i n n a t u r e , E n c e l i a i s common on sandy s o i l s and the i n h i b i t o r y e f f e c t t h e r e f o r e i s t o be e x p e c t e d . These a u t h o r s , however, d i d not a s s e s s the r e s p o n s e t o the p h y t o t o x i n of such a n n u a l s as were a b s e n t from the v i c i n i t y o f E n c e l i a . Nor d i d t h e y attempt t o i s o l a t e the



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0 1. 8 - c i n e o l e

a-pinene

camphor

COCH.,

CHO OCH 0-pinene

Figure

j.H

C0 H 2

3

3-acetyl-6-methoxybenzaldehyde

1·

W

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A l l e l o c h e m i c a l s from V a r i o u s D e s e r t P l a n t s .



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p h y t o t o x i n from s o i l s around t h e s e s h r u b s . I n t e r e s t i n g l y , l e a v e s o f E n c e l i a c o l l e c t e d i n A r i z o n a y i e l d e d a d i f f e r e n t , as y e t unidentified toxin (3). Guayule ( P a r t h e n i u m argentatum, Compositae), a r u b b e r p r o d u c i n g p l a n t , i s common i n t h e Chihuahua D e s e r t (Mexico and South T e x a s ) , where s p a r s e p o p u l a t i o n s of t h i s shrub grow a t an a l t i t u d e of 700-3500 m above sea l e v e l , r e c e i v i n g 250 mm of a n n u a l r a i n f a l l ( 4 ) . When t h i s p l a n t was grown under n u r s e r y c o n d i t i o n s , m a r g i n a l rows p r o d u c e d l a r g e r p l a n t s t h a n rows i n the c e n t e r , and r o o t s o f one p l a n t d i d not i n t e r m i n g l e w i t h those o f n e i g h b o r i n g plants· From g r a v e l c u l t u r e s w i t h Hoagland s o l u t i o n , Bonner and G a l s t o n (5) i s o l a t e d t r a n s - c i n n a m i c a c i d ( F i g u r e 1), which was found a u t o t o x i c t o g u a y u l e s e e d l i n g s grown i n s i m i l a r g r a v e l c u l t u r e . The a u t o t o x i c 3

e f f e c t was s t i l l e v i d e n t even a t c o n c e n t r a t i o n s of 6.7 χ 10~ mM, and a t 1 mM i t caused an 80-90% r e d u c t i o n i n growth of guayule s e e d l i n g s . Subsequent attempts t o i s o l a t e t h i s o r o t h e r p h y t o t o x i c compounds from v a r i o u s s o i l s s u p p o r t i n g guayule p r o v e d u n s u c c e s s f u l (6,7) . In a s e r i e s of p a p e r s p u b l i s h e d d u r i n g the 1960's, C. H. M u l l e r (8-11) r e p o r t e d t h a t i n a r e a s around shrubs o f S a l v i a leucophylla, S. apiana, S. m i l l i f e r a ( L a b i a t a e ) , or A r t e m i s i a californica (Compositae), g r a s s e s and h e r b s a r e s u p p r e s s e d . The p e r t i n e n t o b s e r v a t i o n s were made i n the Santa Ynez V a l l e y o f Santa B a r b a r a County, C a l i f o r n i a , a r e g i o n w i t h an average a n n u a l r a i n f a l l o f 200-250 mm. Zones e n t i r e l y d e v o i d o f a n n u a l p l a n t s o c c u r r e d w i t h i n 60-90 cm from the canopy of each shrub, whereas f u r t h e r o u t , t o about 6 m, v a r i o u s g r a d a t i o n s of i n h i b i t i o n were o b s e r v e d . V o l a t i l e m a t e r i a l s from the c r u s h e d l e a v e s o r t w i g s of t h e named shrubs i n h i b i t e d r o o t growth i n s e e d l i n g s o f cucumber o r o a t s , as w e l l as of some a n n u a l s common i n the a r e a . H i g h e s t i n h i b i t i o n was e x e r t e d by A r t e m i s i a c a l i f o r n i c a , w h i l e no i n h i b i t i o n was o b t a i n e d w i t h m a c e r a t e d young o r mature r o o t s o f S a l v i a l e u c o p h y l l a or t h e i r l e a c h a t e s (10) · S e v e r a l t e r p e n e s and t e r p e n o i d s , e.g. a-pinene, β - p i n e n e , camphor, and c i n e o l e , r e l e a s e d from t h e shrubs canopy were i d e n t i f i e d ( F i g u r e 1 ) . Of t h e s e , camphor d i s p l a y e d the h i g h e s t t o x i c i t y . The agent t r a n s p o r t i n g the p h y t o t o x i n s i n t o the s o i l was f i r s t assumed t o be dew (9) but s u b s e q u e n t l y i t was shown t h a t d r y , r a t h e r t h a n wet, s o i l s a b s o r b e d more o f the v o l a t i l e p h y t o t o x i n s and t h e s e p r o v e d t o be t o x i c f o r the s e e d l i n g s o f a n n u a l s common i n the r e g i o n s s t u d i e d (11) · T h i s l e d t o the c o n j e c t u r e t h a t v o l a t i l e compounds accumulate i n the s o i l d u r i n g the l o n g dry summer and i n the w i n t e r , when g e r m i n a t i o n commences, t o be r e l e a s e d by r a i n f a l l i n t o the s o i l m i c r o s p h e r e , where they i n h i b i t growth o f the a n n u a l s (12) . A l l e l o p a t h y i n Deserts

o f the E a s t e r n Hemisphere

In t h e Negev D e s e r t o f I s r a e l , near Sede Boquer, w i t h i n a r e g i o n b o a s t i n g up t o 100 mm of r a i n f a l l p e r y e a r ( F i g u r e 2 ) , Friedman e t a l . (13) o b s e r v e d t h a t on s o u t h - f a c i n g s l o p e s the y i e l d of a n n u a l s was 6-8 times t h a t on a d j a c e n t n o r t h - f a c i n g s l o p e s ( F i g u r e 3 ) . T h i s was c o n f i r m e d b o t h by the a n n u a l - p l a n t s d e n s i t y and by the dry m a t t e r y i e l d (g/m ), and p r o v e d t r u e d u r i n g 4 y e a r s , d e s p i t e the 2


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Allelopathy

Figure

2.

Map showing L o c a t i o n o f the Study Area Isohyetal Lines.

Including



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ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

F i g u r e 3.

Annual Y i e l d o f Annuals on Southern and N o r t h e r n S l o p e s i n Sede Boquer, i n t h e Years 1964-1967.



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f a c t t h a t the s o u t h - f a c i n g s l o p e s a r e much more a r i d t h a n t h e n o r t h - f a c i n g ones (due t o h i g h s o l a r r a d i a t i o n , h i g h e r s a l i n i t y , and h i g h e r water run-off)· I t was n o t e d , however, t h a t t h e n o r t h - f a c i n g s l o p e s are dominated by the a r o m a t i c semi-dwarf shrub A r t e m i s i a h e r b a - a l b a (Compositae) ( F i g u r e s 4a & b ) , whereas t h e s o u t h - f a c i n g ones are dominated by a nonaromatic shrub ( Zygophyllum dumpsurn , Z y g o p h y l l a c e a e ) ( F i g u r e 5 ) . One y e a r f o l l o w i n g removal o f p e r e n n i a l s from b o t h s l o p e s , the y i e l d o f a n n u a l s on the n o r t h e r n s l o p e i n c r e a s e d s i g n i f i c a n t l y ( F i g u r e s 6a & b ) , a l b e i t i t d i d n o t match t h a t on the p e r e n n i a l - f r e e s o u t h e r n s l o p e . Counts made d u r i n g g e r m i n a t i o n time showed t h a t d e n s i t y of the s e e d l i n g s o f a n n u a l s i n the v i c i n i t y o f A r t e m i s i a h e r b a - a l b a was o n l y h a l f t h a t o b s e r v e d 100 cm from the canopy. On the s u s p i c i o n t h a t v o l a t i l e a l l e l o c h e m i c a l s were r e s p o n s i b l e f o r the d e c i m a t i o n o f a n n u a l s on the n o r t h - f a c i n g s l o p e s , l a b o r a t o r y t e s t s were u n d e r t a k e n u s i n g s m a l l p l a s t i c b e a k e r s ( F i g u r e 7 ) . These t e s t s c o n f i r m e d t h a t Artemisia h e r b a - a l b a , l i k e A. c a l i f o r n i c a , produces v o l a t i l e phytotoxins. Thus, one gram o f f r e s h shoots o f _A^ herba-alba i n a s e a l e d 50-ml f l a s k a r r e s t e d the g e r m i n a t i o n o f v a r i o u s a n n u a l s p e c i e s common i n the s t u d i e d a r e a , whereas no such i n h i b i t i o n was i n d u c e d by the l e a v e s o f Zygophyllum used as a c o n t r o l ( 1 3 ) . Of the s p e c i e s examined f o r g e r m i n a t i o n i n h i b i t i o n , S t i p a c a p e n s i s and Helianthemum l e d i f o l i u m were s t r o n g l y i n h i b i t e d , Zygophyllum dumosum l e s s so, and the two v a r i e t i e s o f Medicago l a c i n i a t a not a t a l l . Major v o l a t i l e i n h i b i t o r s t u r n e d out t o be t e r p e n e s and t e r p e n o i d s , such as α - p i n e n e , camphor, and c i n e o l e ( F i g u r e 1 ) . We then p o s t u l a t e d t h a t chemical i n h i b i t i o n i s mainly r e s p o n s i b l e f o r the absence or s c a r c i t y of s e n s i t i v e s p e c i e s i n the v i c i n i t y o f A r t e m i s i a and t h a t the y i e l d o f a n n u a l s on p l o t s f r e e o f p e r e n n i a l s on the l e s s a r i d n o r t h - f a c i n g s l o p e s does not exceed the y i e l d on the s o u t h e r n s l o p e s owing t o p e r s i s t e n c e o f r e s i d u a l p h y t o t o x i n s i n the s o i l . A l l our attempts t o demonstrate s o i l t o x i c i t y by sampling o f s o i l s i n p o t s f a i l e d , p r o b a b l y because o f the v o l a t i l e n a t u r e o f the phytotoxins· When shoots of A r t e m i s i a herba-alba c o l l e c t e d i n the d e s e r t were p l a c e d near seeds o f v a r i o u s a n n u a l p l a n t s , g e r m i n a t i o n was i n h i b i t e d and such i n h i b i t i o n was h i g h l y reproducible. However, when p l a n t s of A. h e r b a - a l b a were t r a n s p l a n t e d i n a more humid r e g i o n i n T e l A v i v , s i m i l a r i n h i b i t o r y e f f e c t s were o b t a i n e d o n l y when 3-4 times as many s h o o t s were applied. Water s t r e s s , h i g h sun r a d i a t i o n , and h i g h t e m p e r a t u r e s a r e b e l i e v e d sometimes t o f a v o r h i g h e r p r o d u c t i o n and r e l e a s e o f v o l a t i l e t e r p e n e s and t e r p e n o i d s . T h i s i s a common, a n c i e n t b e l i e f among m i n t growers which g a i n e d s u p p o r t from the work o f C l a r k and Manary (14) . I n t e r e s t i n g l y , our o b s e r v a t i o n s on p o p u l a t i o n s of Artemisia h e r b a - a l b a i n l e s s a r i d r e g i o n s i n I s r a e l ( a l b e i t w i t h no more t h a n 350 mm of a n n u a l r a i n f a l l ) not o n l y f a i l e d t o show any r e d u c t i o n i n the number o f nearby a n n u a l s , but a c t u a l l y r e v e a l e d t h a t a n n u a l s may a g g r e g a t e around t h e A r t e m i s i a p l a n t s . In g e n e r a l , one would e x p e c t the degree o f i n h i b i t i o n t o depend b o t h on the s u s c e p t i b i l i t y o f d i f f e r e n t p l a n t s p e c i e s as w e l l as on the r e a c t i v i t y of the i n h i b i t o r s , t h e i r c o n c e n t r a t i o n and t h e i r p r o x i m i t y t o the s u s c e p t i b l e p l a n t . P o p u l a t i o n s of _Aj_ herba-alba 2

a r e r e l a t i v e l y dense (about 3 p l a n t s / m ) and the shrubs a r e e x t r e m e l y a r o m a t i c , p a r t i c u l a r l y d u r i n g the l o n g summer




F i g u r e 4.

Artemisia (b) .

herba-alba

, Branch (a) and

Inflorescences



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F i g u r e 5.

Figure

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A r t e m i s i a h e r b a - a l b a on a N o r t h - f a c i n g S l o p e (bottom) and Zygophyllum dumpsum on a S o u t h - f a c i n g S l o p e (top).

a. A f l a s h o f a n n u a l s on a n A r t e m i s i a - f r e e p l o t ( l e f t ) compared w i t h t h o s e o f an u n d i s t u r b e d p l o t u s e d as a c o n t r o l ( r i g h t ) , 8 months a f t e r removal o f t h e A r t e m i s i a shrubs. ( R e p r o d u c e d w i t h p e r m i s s i o n f r o m r e f e r e n c e 13. C o p y r i g h t 1977 B l a c k w e l l S c i e n t i f i c P u b l i c a t i o n s L t d . )



62


F i g u r e 6.

b . Mature P l a n t s o f I f l o g a s p i c a t a Sampled from t h e A r t e m i s i a - f r e e P l o t ( l e f t ) and from t h e U n d i s t u r b e d Plot (right).

F i g u r e 7.

P o l y t h e n e Beaker Used i n G e r m i n a t i o n Experiments : A, P l a s t i c c o v e r ; B, Seeds; C, F i l t e r Paper; D, Open b e a k e r employed i n t h e " v o l a t i l e s method" (13) (by p e r m i s s i o n o f B l a c k w e l l S c i e n t i f i c Publications)·



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(May-October), when the upper s o i l l a y e r may a d s o r b i n h i b i t o r s t o the p o i n t of s a t u r a t i o n . In such a c a s e , a r a i n f a l l of 100 mm p e r annum, such as o c c u r s on the s l o p e s and p a r t o f which (10-30%) d i s a p p e a r s q u i c k l y as r u n - o f f , would be u n l i k e l y t o d e p l e t e the s o i l of i n h i b i t o r s by l e a c h i n g . V a r i a b l e e c o l o g i c a l c o n d i t i o n s may t r i g g e r a l l e l o p a t h y o f A. h e r b a - a l b a i n one h a b i t a t and a b r o g a t e i t i n the n e x t one. The wide g l o b a l d i s t r i b u t i o n o f A. herba-alba from N o r t h A f r i c a t o the I r a n i a n d e s e r t s s u g g e s t s t h a t the a l l e l o p a t h i c phenomenon a s s o c i a t e d w i t h t h i s s p e c i e s may m a n i f e s t a l s o i n geographic regions other than i n I s r a e l . In the r e g i o n s t u d i e d , n e a r Sede Boquer, dwarf shrubs o f Artemisia h e r b a - a l b a d i s p e r s e 85% of t h e i r d i a s p o r e s (achenes) under the canopy and y e t most o f the g e r m i n a t i o n t a k e s p l a c e o u t s i d e the s h r u b s canopy (15) · T h i s i s t r u e even though the canopy of A. h e r b a - a l b a p r o v i d e s b o t h shade and l i t t e r d u r i n g the g e r m i n a t i o n p e r i o d , so t h a t h u m i d i t y under the shrubs i s b e l i e v e d t o be h i g h e r t h a n o u t s i d e i t . P o p u l a t i o n r e g u l a t i o n by a u t o t o x i c i t y i s t h u s s u g g e s t e d . Our f i e l d o b s e r v a t i o n s f u r t h e r s u g g e s t the o c c u r r e n c e o f s i m i l a r i n t e r a c t i o n s between the p a r e n t p l a n t and i t s seeds and s e e d l i n g s ( p r o b a b l y by the s h r u b s ' l i t t e r ) i n the case of the sand-dune-located non-aromatic A r t e m i s i a monosperma. 1

Tamarix a p h y l l a (Tamaricaceae) i s a t r e e of moderate h e i g h t (8-11 m). In I s r a e l i t i s p r e v a l e n t i n the c o a s t a l p l a i n and i n t h e Negev d e s e r t . I t n o r m a l l y grows i n x e r i c a r e a s w i t h 100 mm of a n n u a l r a i n f a l l (16) and i s r e c o g n i z e d as a s a l t - e x c r e t i n g t r e e ( 1 7 ) . L i t w a k i n 1957 (18) s t u d i e d the i n f l u e n c e of t h i s t r e e on soil salinization. At t h a t time he n o t i c e d t h a t i n a r i d l o c a l i t i e s w i t h l e s s t h a n 200 mm of a n n u a l r a i n f a l l no p l a n t s o f any k i n d grew under the c a n o p i e s o f the l a r g e t r e e s , even i n r a i n y y e a r s . At the p e r i p h e r y and s t i l l under the p a r t i a l i n f l u e n c e of the l i t t e r and water d r i p p i n g from the canopy, some h a l o p h y t i c and r u d e r a l s p e c i e s appeared, e.g. B a s s i a muricata, Mesembryanthemum n o d i f l o r u m , o r Chenopodium o p u l i f o l i u m ( F i g u r e s 8a, b ) . Compared w i t h s o i l samples from the open a r e a , t h o s e from under the canopy c o n t a i n e d t w i c e as many s o l u b l e s a l t s ( T a b l e I ) . TABLE I . T o t a l S o l u b l e S a l t s under the Canopy o f O l d T r e e s of Tamarix a p h y l l a and out i n the Open (average v a l u e s , Depth (cm) 0 40 80

Under the (a) 1201 1198 859

+ + +

canopy

345 216 187

In the open (b) 480 512 490

+ + +

Source: Reproduced w i t h p e r m i s s i o n from R e f . The tfeizmann S c i e n c e P r e s s o f I s r a e l ,

120 102 78 18.

ppm)

a/b

2.5 2.3 1.7 Copyright

1957

Under s m a l l t r e e s o f Ί\_ a p h y l l a (3-5 m i n h e i g h t ) , a n n u a l s were not e n t i r e l y a b s e n t . To e v a l u a t e the e f f e c t of the t r e e s on a n n u a l s , a l o n g a d i s t a n c e g r a d i e n t from the stem, we d e t e r m i n e d b o t h the d e n s i t y o f



64


F i g u r e 8.

F i g u r e 8.

a . A n n u a l s - f r e e Areas around T r e e s o f Tamarix aphylla, 15 km South o f Beer Sheva ( c f . F i g . 2 ) .

b . H a l o p h y t e s and R u d e r a l s (HR) i n t h e P e r i p h e r y o f an A n n u a l s - f r e e Area around Tamarix aphylla.


6.

Allelopathy

FRIEDMAN

in Desert

65

Ecosystems +

a n n u a l s and the c h l o r i d e ( C l ~ ) and sodium (Na ) c o n c e n t r a t i o n s i n t h e upper s o i l l a y e r (0.5 cm), p r o c e e d i n g s e r i a t i m from the stem towards t h e p e r i p h e r y of the t r e e . The d a t a p r e s e n t e d i n F i g u r e 9 show t h a t c l o s e t o t h e stem t h e C l ~ c o n c e n t r a t i o n i s h i g h e s t , and the a n n u a l s d e n s i t y l o w e s t , but the s i t u a t i o n r e v e r s e s towards the


+

tree's periphery. A s i m i l a r p a t t e r n was o b s e r v e d a l s o f o r t h e N a c o n c e n t r a t i o n i n the upper s o i l l a y e r v i s - a - v i s the a n n u a l s d e n s i t y . Sodium c h l o r i d e i s the major s a l t e x c r e t e d by Tamarix aphylla. However, the c o m p o s i t i o n o f the e x c r e t e d s a l t s i s t o a c e r t a i n e x t e n t i n f l u e n c e d by the c o m p o s i t i o n o f t h e s a l t s e n c o u n t e r e d by t h e r o o t s (19) . The r a t e o f e x c r e t i o n of sodium c h l o r i d e , when measured i n r e l a t i o n t o i t s c o n c e n t r a t i o n around t h e r o o t system, shows an optimum p a t t e r n , i . e . h i g h e s t a t a 0.2 M c o n c e n t r a t i o n and d i m i n i s h i n g when the r o o t s a r e i r r i g a t e d w i t h e i t h e r lower o r h i g h e r c o n c e n t r a t i o n s o f sodium c h l o r i d e (19) · The marked a l l e l o p a t h i c e f f e c t i n the more a r i d r e g i o n s i s p r o b a b l y due t o a c o m b i n a t i o n o f t h e f o l l o w i n g : t h e e c o l o g i c a l c o n d i t i o n s , the f a c t t h a t the s o i l s i n t h e s e a r e a s a r e s u f f i c i e n t l y s a l i n e t o enhance t h e r a t e o f s a l t e x c r e t i o n by the t r e e s , and the a n n u a l r a i n f a l l is insufficinent t o wash t h e e x c r e t e d s a l t s i n t o lower s a l t l a y e r s . I t seems t h a t t h i s a l l e l o p a t h i c e f f e c t i s a s e c o n d a r y e v e n t r e s u l t i n g from the e x c r e t i o n mechanism o f t a m a r i s k s which removes t h e s a l t s from t h e r o o t s , s u b s e q u e n t l y e l i m i n a t i n g them by the s a l t g l a n d s and f i n a l l y c o n c e n t r a t i n g them i n the upper s o i l l a y e r around t h e c a n o p i e s . The c o n t r i b u t i o n of t h i s a l l e l o p a t h i c e f f e c t t o the s u r v i v a l o f the species i s doubtful. T r e e s o f T. a p h y l l a were f o u n d t o be s u s c e p t i b l e t o sodium c h l o r i d e even when i r r i g a t e d w i t h as l i t t l e as 0.1 M N a C l (19) · I t i s n o t s u r p r i s i n g , t h e r e f o r e , t h a t i n t h e a n n u a l - f r e e c o n c e n t r i c a r e a s under the c a n o p i e s , we c o u l d not f i n d any r o o t s o f t a m a r i s k c a p a b l e o f e x p l o i t i n g the n o n - u t i l i z e d w a t e r . Nevertheless, i t i s c l e a r that inorganic minerals of p l a n t o r i g i n can i n d u c e a l l e l o p a t h y . Indeed, i n the case o f C e r a t o p h y l l u m demersum e l e m e n t a l s u l f u r was r e c e n t l y found a c c o u n t a b l e f o r the f a c t t h a t v e r y few e p i p h y t e s a s s o c i a t e w i t h t h i s water p l a n t (20) · I t i s p o s s i b l e t h a t o t h e r t r e e s o r shrubs a c t i v e i n t h e s a l i n i z a t i o n p r o c e s s o f s o i l s o r a f f e c t s o i l pH, e. g. S a r c o b a t u s vermiculatus (Chenopodiaceae) i n E s c a l e n t e D e s e r t , Utah (21) may under s p e c i f i c e c o l o g i c a l c o n d i t i o n s induce a l l e l o p a t h i y . Discussion

and

Conclusions

From t h e accumulated i n f o r m a t i o n on a l l e l o p a t h y o r a u t o t o x i c i t y i n a r i d r e g i o n s of b o t h hemispheres, some g e n e r a l i z a t i o n s may be drawn: (a) a g g r e s s i v e p l a n t s w i t h a l l e l o p a t h i c p o t e n t i a l are a d u l t p e r e n n i a l s o r young s e e d l i n g s o f such p e r e n n i a l s ; (b) the a l l e l o c h e m i c a l s a r e e i t h e r common s e c o n d a r y m e t a b o l i t e s or i n o r g a n i c s a l t s . They a r e o f t e n n o n s p e c i f i c , n o t g e n e r a l p h y t o c i d e s . They r e a c h the s u s c e p t i b l e p l a n t t h r o u g h t h e s o i l i n v a r i o u s ways - by b e i n g washed o f f d u r i n g r a i n f a l l from t h e f r e s h o r d r i e d l e a v e s and stems, by e s c a p i n g as v o l a t i l e s u b s t a n c e s from t h e s h o o t s t o be a d s o r b e d l a t e r by the s o i l , o r by l i b e r a t i o n from t h e mature o r decomposed r o o t s t o r e a c h t h e r o o t l e t s o f t h e young p l a n t ;



66


canopy

F i g u r e 9.

—>j

radius

Annuals D e n s i t y (o) and C h l o r i d e C o n c e n t r a t i o n ( A ) a t V a r i o u s D i s t a n c e s from Stem t o P e r i p h e r y o f Tamarix a p h y l l a (mean v a l u e s o f 5 t r e e s ) . D i s t a n c e s e x p r e s s e d as f r a c t i o n o f t h e t r e e s radii. 1



6.

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67

(c) the a l l e l o c h e m i c a l e f f e c t i s s u b j e c t t o l o c a l s m a l l - s c a l e changes as w e l l as t o l a r g e g e o g r a p h i c a l ones. V e r y few a n n u a l s , f o r i n s t a n c e , a r e a s s o c i a t e d w i t h shrubs of Artemisia h e r b a - a l b a on the h i l l s l o p e s o f the Negev D e s e r t , but t h i s i s not so i n the r u n n e l s or i n l e s s a r i d n o r t h e r n r e g i o n s , f o r t r a n s p l a n t a t i o n of t h e p l a n t s from t h e dry d e s e r t c l i m a t e t o the w e t t e r M e d i t e r r a n e a n , one r e d u c e s the p r o d u c t i o n o f v o l a t i l e p h y t o t o x i n s . I t i s t h e r e f o r e s u g g e s t e d t h a t a r i d r e g i o n s t h a t m a n i f e s t an a r i d i t y g r a d i e n t a r e f i t t e d f o r the e x p l o r a t i o n of new a l l e l o p a t h i c e f f e c t . C l e a r l y , a l l e l o p a t h y i s more common under d e s e r t c o n d i t i o n s t h a n i n humid e n v i r o n m e n t s . T h i s i s not because the wide s p a c i n g s between the p l a n t s i n the d e s e r t a l l o w an e a s i e r d e t e c t i o n of the a l l e l o p a t h i c e f f e c t , b u t because t h e r e a r e e c o l o g i c a l c o n d i t i o n s t h a t f a v o r a l l e l o p a t h y , such as t h o s e a f f e c t i n g the r a t e o f p r o d u c t i o n o f a l l e l o c h e m i c a l s o r d e t e r m i n i n g the e f f e c t i v e n e s s o f the a l l e l o c h e m i c a l s a l r e a d y i n the s o i l . Among f u r t h e r f i n d i n g s o f the p r e s e n t study a r e t h e f o l l o w i n g : 1· Water and n u t r i e n t s t r e s s may o f t e n i n c r e a s e a l l e l o c h e m i c a l production. In a r e c e n t r e v i e w , Gershenzon (22) has p o i n t e d o u t t h a t numerous a l l e l o c h e m i c a l s o f v a r i o u s c h e m i c a l groups a r e o f t e n p r o d u c e d and s t o r e d i n much h i g h e r c o n c e n t r a t i o n s by p l a n t s under water o r n u t r i e n t s t r e s s t h a n by p l a n t s growing under o p t i m a l conditions· 2. There i s some e v i d e n c e t h a t g r a z i n g can a l s o t r i g g e r the p r o d u c t i o n o f a l l e l o c h e m i c a l s (23-25) , a l b e i t t h i s was r e p o r t e d f o r o n l y a few p l a n t s and was n o t s t u d i e d a t a l l i n d e s e r t p l a n t s . F u t u r e i n v e s t i g a t i o n may perhaps r e v e a l t h a t the g r a z i n g e f f e c t i m p o r t a n t l y a g g r a v a t e s a l l e l o p a t h y i n the d e s e r t s . 3. A l l e l o c h e m i c a l s i n d e s e r t s o i l s a r e p r e d i c t a b l y l e s s prone t o l e a c h i n g and r a p i d biodégradation t h a n a r e s o i l s i n humid environments· 4. Sandy s o i l s , w i t h low amounts o f o r g a n i c m a t t e r , a r e most common i n d e s e r t s . As such, t h e y may r e l e a s e the a d s o r b e d c h e m i c a l s more r e a d i l y t h a n w i l l heavy s o i l s r i c h i n o r g a n i c m a t t e r . As i n o t h e r e n v i r o n m e n t s , so a l s o i n a r i d r e g i o n s , a l l e l o p a t h y i s a s s o c i a t e d w i t h p l a n t - p l a n t c o m p e t i t i o n , but here the p a u c i t y of r e s o u r c e s may l e a d t o c o n s i d e r a b l e mutual i n t e r f e r e n c e r e s u l t i n g not o n l y i n d i m i n u t i o n i n s i z e o r number of the p l a n t s , but a l s o i n t o t a l e x t i n c t i o n of a v u l n e r a b l e s p e c i e s . T h i s does not mean t h a t a n a l y s i s o f a l l e l o p a t h y i n an a r i d environment s h o u l d be done d i f f e r e n t l y from t h a t which i s customary i n a humid environment; y e t i t i s i m p o r t a n t t o e s t i m a t e the e x t e n t t o which i n o r g a n i c s a l t s ( e x c r e t e d by the p l a n t o r r e l e a s e d from i t s l i t t e r ) a r e i n v o l v e d i n the a l l e l o p a t h i c e f f e c t . So f a r as s e c o n d a r y m e t a b o l i t e s a r e c o n c e r n e d , i t s h o u l d be o f i n t e r e s t t o compare t h e i r p r o d u c t i o n under humid and s t r e s s e d c o n d i t i o n s . It i s s u g g e s t e d t h a t f o r the e v a l u a t i o n o f the a l l e l o c h e m i c a l e f f e c t , s p e c i e s s u p p r e s s e d i n t h e i r n a t u r a l h a b i t a t s h o u l d be p r e f e r r e d o v e r any o t h e r s t a n d a r d seeds commonly u s e d f o r e v a l u a t i n g g e r m i n a t i o n i n h i b i t o r s . A l s o , e f f o r t s t o i s o l a t e a l l e l o c h e m i c a l s from s o i l s w i l l a s s i s t i n the e s t a b l i s h m e n t o f a l l e l o p a t h y on a more c o n c r e t e b a s i s than i s a v a i l a b l e at present.


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5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21 22. 23. 24. 25.

Went, F. W. Bull. Torrey Bot. Club, 1942, 39, 100-114. Gray, R.; Bonner, J . Am. J . Bot., 1948, 35, 52-57. Gray, R.; Bonner, J . J . Am. Chem. Soc. 1948, 70, 1249-1253. Lloyd, F. E. "Guayule ( Parthenium argentatum Gray); A rubber-plant of the Chihuahuan Desert". Carnegie Institute of Washington, 1911, 213 pp. Bonner, J.; Galston, A. W. Bot. Gaz. (Chicago) 1944, 106, 185-198. Bonner, J . Bot. Gaz. (Chicago) 1946, 107, 343-351. Bonner, J . Bot. Rev., 1950, 16, 51-65. Muller, C.-H.; Chou, C. H. In "Phytochemical Ecology"; Harborne, J. B., Ed.; Academic Press: London, 1972; pp. 201-216. Muller, C. H.; Muller, W. H.; Haines, B. L. Science, 1964, 143, 471-473. Muller, W. H.; Muller, C. H. Bull. Torrey Bot. Club, 1964, 91, 327-330. Muller, C. H.; del Moral, R. Bull. Torrey Bot. Club, 1964, 93, 130-136. Halligan, J . P. Am. Midi. Nat. 1976, 95, 406-421. Friedman, J.; Orshan, G.; Ziger-Cfir, Y. J . Ecol. 1977, 65, 413-426. Clark, R. J.; Menary, R. C. Aust. J . Agricul. Res. 1980, 31, 489-498. Friedman, J., Orshan, G. J. Ecol. 1975, 63, 627-632. Friedman, J., Waisel, Y. La-Yaaran (The Forester) 1964, 13, 156-161. Volkens, G. "Die Flora der Aegyptisch-Arabischen Weste auf lage Grundanatomisch-physiologischen Untersuchungen", Berlin, Gebr. Borntraeger: Berlin, 1887; pp. 156, tab 18. Litwak, M. Bull. Res. Counc. Israel, 1957, 6D, 38-45. Waisel, Y. Plant and Soil, 1961, 13, 356-364. Wium-Andersen, S.; Antoni, U.; Houen, G. Phytochemistry, 1983, 22(11), 2613. Fireman, M.; Hayward, H. E. Utah Bot. Gaz. 1952. 114, 2. Gershenzon, J . In "Recent Advances in Phytochemistry"; Timmermann, N.; Steelnik, G.; Loewus, F. Α., Eds.; Plenum Press: New York, London, 1984; pp. 273-320. Green, T. R.; Rayan, C. A. Science, 1972, 175, 776-777. Loper, G. M. Crop Sc., 1968, 8, 104-106. Schultz, J . C.; Baldwin, I. T. Science, 1982. 217, 149-151.

RECEIVED

December 23,1985


Allelopathy in Desert Ecosystems - ACS Symposium Series (ACS

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