On Certain Unifying Principles in Ecology R. Margalef The American Naturalist, Vol. 97, No. 897. (Nov. - Dec.

, 1963), pp. 357-374.

Stable URL: http://links.jstor.org/sici?sici=0003-0147%28196311%2F12%2997%3A897%3C357%3AOCUPIE%3E2.0.CO%3B2-1 The American Naturalist is currently published by The University of Chicago Press.

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THE

AMERICAN NATURALIST

Vol. S C V I I November-December, 1 9 6 3 No. 8 9 7

ON CERTAIN UNIFYING PRINCIPLES IN ECOLOGY

R. MARGALEF

I n s t i t u t e for F i s h e r i e s I n v e s t i g a t i o n , B a r c e l o n a , Spain

Ecologists have been reluctant t o place their observations and their f i n d i n g s i n t h e frame of a g e n e r a l theory. P r e s e n t day e c o l o g y i s extremely poor i n unifying a n d ordering p r i n c i p l e s . h c e r t a i n effort s h o u l d b e m a d e i n c o n s t r u c t i n g a g e n e r a l frame of r e f e r e n c e , e v e n though s o m e of t h e s p e c u l a t i o n may b e d a n g e r o u s or m i s l e a d i n g . T h i s p a p e r p r e s e n t s v a r i o u s p o i n t s of v i e w , s o m e p e r h a p s o r i g i n a l , o t h e r s n o t s o . C e r t a i n of t h e s e v i e w p o i n t s h a v e b e e n d i s c u s s e d p r e v i o u s l y but s e p a r a t e l y , in o t h e r p a p e r s p u b l i s h e d or i n p r e s s . In s u c h a n e n t e r p r i s e , d i s c u s s i o n with s t u d e n t s a n d c o l l e a g u e s h a s b e e n e s s e n t i a l , a n d t h e a u t h o r h a s profited from t h e e x p e r i e n c e a n d c r i t i c i s m of many p e o p l e . A s p e c i a l s e n s e of i n d e b t e d n e s s i s f e l t t o w a r d s Monte L l o y d , H. T . Odurn, R . biacArthur, E. P. Odum, G. E . H u t c h i n s o n , a n d V. T o n o l l i .
STRUCTURE O F T H E ECOSYSTEM

E c o s y s t e m s h a v e a s t r u c t u r e , i n t h e s e n s e t h a t t h e y a r e c o m p o s e d of different p a r t s or e l e m e n t s , a n d t h e s e a r e a r r a n g e d i n a d e f i n i t e p a t t e r n . T h e i n t e r r e l a t i o n s b e t w e e n t h e c o n s t i t u e n t e l e m e n t s a r e t h e b a s i s of t h e s t r u c t u r e . Of c o u r s e , i t i s p o s s i b l e t o r e c o g n i z e a n d m e a s u r e different deg r e e s of s t r u c t u r e . O n e m e a s u r e would b e t h e number of p a r a m e t e r s n e e d e d for d e s c r i b i n g a c e r t a i n s i t u a t i o n . More s p e c i f i c a l l y , e c o s y s t e m s formed by a g r e a t e r number of s p e c i e s all o w for a h i g h e r number of s p e c i f i c r e l a t i o n s i n food w e b s , p a r a s i t i s m , e t c . T h e s e r e q u i r e a longer d e s c r i p t i o n , t o e x p r e s s a n e q u i v a l e n t d e g r e e o f knowledge. C o n s i d e r i n g t h e e c o s y s t e m i n t e r m s of i n d i v i d u a l s d i s t r i b u t e d i n different s p e c i e s i s only o n e of s e v e r a l p o s s i b i l i t i e s ; we c a n think of i t a l s o i n r e l a t i o n t o c h e m i c a l compounds or b i o c h e m i c a l s y s t e m s . F o r example, a s s i m i l a t o r y p i g m e n t s provide a v e r y c o n c r e t e a n d u s e f u l b o t a n i c a l a p p r o a c h . A s i m i l a r c o n c e p t of s t r u c t u r e c a n b e a p p l i e d e v e n t o t h e environment. C o n s i d e r , for i n s t a n c e , t h e k i n d s a n d proportions of o r g a n i c s u b s t a n c e s produced by o r g a n i s m s a n d p r e s e n t i n a q u a t i c e c o s y s t e m s . T h e main p o i n t is t h a t t h e "real" s t r u c t u r e of a n e c o s y s t e m i s a property t h a t r e m a i n s o u t of r e a c h , but t h i s c o m p l e t e s t r u c t u r e i s r e f l e c t e d in many a s p e c t s of t h e e c o s y s t e m t h a t c a n b e s u b j e c t e d t o o b s e r v a t i o n : i n t h e d i s -

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T H E AMERICAN N A T U R A L I S T

tribution of i n d i v i d u a l s i n t o s p e c i e s , i n t h e p a t t e r n of t h e food n e t , i n t h e d i s t r i b u t i o n of t o t a l a s s i m i l a t o r y p i g m e n t s i n k i n d s of p i g m e n t s , a n d s o on. Structure, i n g e n e r a l , b e c o m e s more c o m p l e x , more r i c h , a s time p a s s e s ; s t r u c t u r e is l i n k e d to h i s t o r y . F o r a q u a n t i t a t i v e m e a s u r e of s t r u c t u r e it s e e m s c o n v e n i e n t t o s e l e c t a name t h a t s u g g e s t s t h i s h i s t o r i c a l c h a r a c t e r , for i n s t a n c e , maturity. In g e n e r a l , we may s p e a k of a more c o m p l e x e c o s y s t e m a s a more mature e c o s y s t e m . T h e term maturity s u g g e s t s a trend, a n d moreover m a i n t a i n s a c o n t a c t with t h e t r a d i t i o n a l d y n a m i c a p p r o a c h i n t h e s t u d y of n a t u r a l c o m m u n i t i e s , w h i c h h a s a l w a y s b e e n a s o u r c e of inspiration. Maturity, t h e n , is a q u a l i t y t h a t i n c r e a s e s with t i m e in a n y u n d i s t u r b e d e c o s y s t e m . F i e l d e c o l o g i s t s u s e many c r i t e r i a t o e s t i m a t e t h e maturity of a n e c o s y s t e m , without t h e n e e d of a s s e s s i n g i t s p r e c i s e p l a c e in a n a c t u a l s u c c e s s i o n . E m p i r i c a l k n o w l e d g e of s u c c e s s i o n l e a d s o n e t o c o n s i d e r a s more mature t h e e c o s y s t e m s t h a t a r e more complex; t h a t i s , c o m p o s e d of a g r e a t number of e l e m e n t s , with l o n g food c h a i n s , a n d with r e l a t i o n s b e t w e e n s p e c i e s w e l l d e f i n e d or more s p e c i a l i z e d . S t r i c t l y s t e n o p h a g o u s a n i m a l s , p a r a s i t e s , a l l s o r t s of v e r y p r e c i s e s y m b i o t i c or d e f e n s i v e r e l a t i o n s , a r e commoner i n mature e c o s y s t e m s . Furthermore, s i t u a t i o n s a r e more predicta b l e , t h e a v e r a g e l i f e of i n d i v i d u a l s i s l o n g e r , t h e number of produced offs p r i n 5 lower, a n d i n t e r n a l o r g a n i z a t i o n of t h e e c o s y s t e m t u r n s random d i s t u r b a n c e s i n t o q u a s i r e g u l a r rhythms. L e a v i n g a s i d e for t h e moment t h e a s p e c t s of turnover a n d rhythms t o b e d e a l t with l a t e r , we c a n f o c u s now on t h e s t r u c t u r e a n d how i t c a n b e e x p r e s s e d q u a n t i t a t i v e l y . Practical situations impose severe limitations on theoretical possibilit i e s . T h e o r e t i c a l l y , i t would b e p o s s i b l e t o c o m p u t e a d i v e r s i t y i n d e x , exp r e s s i n g t h e d i s t r i b u t i o n s of i n d i v i d u a l s i n t o s p e c i e s i n t h e whole e c o s y s tem. T h i s is m o s t c o n v e n i e n t l y d o n e by d e t e r m i n i n g t h e a v e r a g e number of b i t s p e r i n d i v i d u a l (Margalef, 1957), but under c o n d i t i o n s t h a t a r e common i n n a t u r a l c o m m u n i t i e s a n y o t h e r d i v e r s i t y i n d e x w i l l b e a p p l i c a b l e . Unf o r t u n a t e l y , nobody h a s e v e n a t t e m p t e d t o u n d e r t a k e a c o m p l e t e c e n s u s of t h e whole community. T h u s , w e a r e forced to c o m p u t e our d i v e r s i t y through s a m p l e s of t h e community, s e l e c t e d by t h e u s e of c e r t a i n t e c h n i c a l implem e n t s (plankton n e t s , t r a p s , l i g h t t o a t t r a c t i n s e c t s ) ur by t a x o n o m i c a l c r i t e r i a ( d i v e r s i t y of b i r d s , of i n s e c t s , of c o p e p o d s , of d i n o f l a g e l l a t e s ) . N e v e r t h e l e s s , t h e r e i s e v i d e n c e t h a t t h e more i n c l u s i v e s t r u c t u r e i s ref l e c t e d i n t h e c o m p o s i t i o n of t h e s e s e l e c t e d p a r t s , arbitrarily c h o s e n by t h e taxonomic r e l a t i o n of c o m p o n e n t s or by m e c h a n i c a l procedure, but a l w a y s m e a s u r e d i n t h e s a m e way. Sampling h a s to b e o r g a n i z e d very c r i t i c a l l y . O n e h a s to remember, for i n s t a n c e , t h a t s a m p l e s i n c l u d i n g s m a l l o r g a n i s m s t a k e n a t random u s u a l l y s h o w a lower d e g r e e of o r g a n i z a t i o n a n d maturity t h a n s a m p l e s of bigger a n i m a l s with d e f i n i t e s p a t i a l p a t t e r n of d i s t r i b u t i o n , a n d with forms of behavior u t i l i z e d by man i n t h e i r c a p t u r e . S a m p l e s t h a t i n c l u d e o r g a n i s m s b e l o n g i n g t o s u p e r i o r t r o p h i c l e v e l s may r e p r e s e n t a higher maturity t h a n s a m p l e s with a more predominant r e p r e s e n t a t i o n of primary p r o d u c e r s .

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On t h e o t h e r h a n d , o n e c a n r e l y on t h e c o n g r u e n c e b e t w e e n e s t i m a t e s of maturity o b t a i n e d a t different l e v e l s . T h e r e i s a good c o r r e l a t i o n b e t w e e n t h e d i v e r s i t y i n t h e d i s t r i b u t i o n of i n d i v i d u a l s into s p e c i e s , a n d i n t h e div e r s i t y o f p l a n t p i g m e n t s i n t h e plankton (Margalef, 1961b). h1acArthur (1961) h a s f o u n d a g o o d c o r r e l a t i o n b e t w e e n bird s p e c i e s d i v e r s i t y , p l a n t s p e c i e s d i v e r s i t y a n d d i v e r s i t y i n t h e m a s s d i s t r i b u t i o n of f o l i a g e of p l a n t s i n different s t r a t a . A g l i m p s e a t t h e f i s h m a r k e t i n a n y p l a c e of t h e world g i v e s a n i d e a of s p e c i e s d i v e r s i t y i n t h e e x p l o i t e d f i s h e r y , a n d i n g e n e r a l , b i o t i c d i v e r s i t y of plankton i n t h e s a m e p l a c e s v a r i e s a c c o r d i n g l y . T h e r e i s n o d o u b t t h a t we c a n g e t numbers e x p r e s s i n g t h e s t r u c t u r e of e c o s y s t e m s . If u s e d properly, t h e s e numbers p e r m i t c o m p a r i s o n s . B'e c a n t e l l w h i c h s y s t e m , of two b e i n g confronted, i s more complex a n d mature. T h i s c a n b e d o n e e i t h e r with neighboring e c o s y s t e m s or with c o m p l e t e l y i n d e p e n d e n t a n d d i s t a n t e c o s y s t e m s . T h e h a n d l i n g of d i v e r s i t y d a t a p o s e s c e r t a i n problems, m o s t l y c o n c e r n e d with t h e s p e c t r u m of d i v e r s i t y i n r e l a tion t o s p a c e , b u t t h e s e q u e s t i o n s h a v e b e e n d i s c u s s e d e l s e w h e r e (Margal e f , 1 9 5 7 , 1 9 6 1 a , 1961b) a n d moreover a r e n o t r e l e v a n t t o t h e p r e s e n t discussion.
THE ECOSYSTEhl IN RELATION TO ENERGY AND MASS

T h e e c o s y s t e m h a s different complementary a s p e c t s : If w e c o n s i d e r t h e e l e m e n t s a n d t h e r e l a t i o n s b e t w e e n t h e e l e m e n t s , we h a v e t h e s t r u c t u r e , w h e r e a s i n c o n s i d e r i n g matter a n d e n e r g y , w e h a v e t o d e a l w i t h m e t r i c p r o p e r t i e s which a r e p e r h a p s e a s i e r t o e x p r e s s . The e c o s y s t e m is formed by a c e r t a i n amount of matter ( b i o m a s s ) and t h e r e i s a budget of matter a n d energy. F o r t h e moment, l e t u s c o n s i d e r an e c o s y s t e m i n a s t e a d y s t a t e , with a m a t e r i a l o u t p u t e q u a l t o t h e m a t e r i a l i n p u t . H e r e w e n e e d to c o n s i d e r o n l y two q u a n t i t i e s : t h e m a t t e r p r e s e n t , or ~ i o m a s s ,i n t h e e c o s y s t e m , a l w a y s t o b e e x p r e s s e d in t h e s a m e form ( t o t a l w e i g h t , dry weight); a n d t h e p o t e n t i a l e n e r g y n e c e s s a r y for m a i n t e n a n c e i n t h e e c o s y s t e m , amounting t o t o t a l r e s piration a n d o t h e r l o s s e s . Both q u a n t i t i e s c a n b e c o n s i d e r e d i n every e c o s y s t e m a n d s i m p l y e q u a t e d t o primary production ( P ) a n d b i o m a s s ( 8 ) ;both c o n c e p t s a r e of common u s a g e i n e c o l o g y . T h e i r r e l a t i o n ( P / B ) c a n b e s t a t e d a s flow of e n e r g y p e r u n i t b i o m a s s ; i t i s t h e turnover r a t e of C u s h i n g , Humphrey, B a n s e a n d L a e v a s t u (1958) a n d t h e productivity i n d e x under n a t u r a l l i g h t c o n d i t i o n s of S t r i c k l a n d (1960). N o t e t h a t i t i s c o n v e n i e n t a l w a y s t o t a k e t h e t o t a l b i o m a s s i n c l u d i n g t h a t of t h e a n i m a l s . T h e dimens i o n s of t h e r a t i o P / D a r e L 2 T d 3 , w h e n P i s e x p r e s s e d a s power; a n d T-' a s s i m p l e turnover. I h e d i m e n s i o n a l q u o t i e n t L - ~ T ' r e p r e s e n t s t h e amount of b i o m a s s n e c e s s a r y t o carry a g i v e n q u a n t i t y of p o t e n t i a l e n e r g y and may c h a n g e from e c o s y s t e m t o e c o s y s t e m . What i s important i s t h e e m p i r i c a l r e l a t i o n b e t w e e n s t r u c t u r e a n d e n e r g y flow p e r u n i t b i o m a s s . More mature e c o s y s t e m s , with a r i c h e r s t r u c t u r e , h a v e a l o w e r primary production p e r unit b i o m a s s . T h i s h a s b e e n o b s e r v e d i n laboratory c u l t u r e s a n d a l l t h e s c a t t e r e d d a t a found i n t h e l i t e r a t u r e

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that seem relevant i n t h i s connection, mostly o n pelagic communities, p o i n t t o w a r d s t h e s a m e c o n c l u s i o n or, a t l e a s t , do not c o n t r a d i c t i t . T h e r a t i o P/B i s t a k e n a s t h e r a t i o e x p r e s s e d by primary productzon/totnl b z o m . r ~ s ,i n c l u d i n g a l l e l e m e n t s of t h e e c o s y s t e m , s u c h a s t h e c o n s u m e r s , e t c . In e c o s y s t e m s of h i g h e r maturity t h e r e i s a more c o m p l e t e u s e of f o o d , t h e r e i s a g r e a t e r proportion of a n i m a l s , a n d e n e r g y c a s c a d e s through a more c o n s i d e r a b l e number of s t e p s . T h i s i s t r u e i n a q u a t i c e c o s y s tems, but in terrestrial e c o s y s t e m s a somewhat paradoxical situation a r i s e s owing t o a c e r t a i n e x a g g e r a t e d d o m i n a n c e of v e g e t a t i o n . On t h e o t h e r h a n d , t h e g r e a t number of p o s s i b l e k i n d s of r e l a t i o n s i n a mature e c o s y s t e m a l l o w s a higher e f f i c i e n c y i n every r e l a t i o n . If t h e s e r e l a t i o n s a r e c o n s i d e r e d a s communication c h a n n e l s , l e s s n o i s e c o m e s i n t o them. T h e r e i s a n o t h e r way to look a t t h e r e l a t i o n s b e t w e e n energy flow p e r u n i t b i o m a s s a n d s t r u c t u r e , b a s e d on a n e x p e r i m e n t t h a t c a n b e i n t r o d u c e d i n e v e r y e c o l o g y c o u r s e . We s t a r t with a n o l d aquarium harboring a mixed population. We c a n m e a s u r e d i v e r s i t y i n t h e d i s t r i b u t i o n of i n d i v i d u a l s i n t o s p e c i e s , a n d i n t h e d i s t r i b u t i o n of p i g m e n t s ; a l s o w e m e a s u r e t o t a l b i o m a s s a n d primary production. T h e r e s u l t s a r e c r i t e r i a for a t t r i b u t i n g to t h e s y s tem, a c e r t a i n q u a n t i t a t i v e e x p r e s s i o n of r a t h e r high maturity. T h e n w e l e a d t h e e c o s y s t e m t o a s t a t e of lower maturity: t h e more e f f e c t i v e w a y of d o i n g t h i s i s t o s t i r t h e c o n t e n t s of t h e aquarium a n d pour i n t o i t s o m e nut r i t i v e s o l u t i o n . We g e t a bloom of plankton a n d t h e s t a t e of l o w e r maturity i s r e f l e c t e d both i n a d e c r e a s e d d i v e r s i t y a t a l l t h e l e v e l s , a n d i n a n i n c r e a s e d r a t i o -przmnry productzon/bzomnss. Of c o u r s e , t h e r e l a t i o n - bzom a s s of p l a n t s / b z o m a s s of nnzmals-changes to t h e b e n e f i t of p l a n t s . T h i s s i m p l e e x p e r i m e n t h a s a c o u n t e r p a r t i n t e r r e s t r i a l e c o l o g y : plowing a f i e l d a n d p u t t i n g manure i n t o i t , a n d t h i s i s o n e of t h e o l d e s t e x p e r i m e n t s i n ecology. If w e w a n t t o follow t h e experiment, w e l e a v e t h e aquarium c o n t a i n i n g our < c r e j u v e n a t e d " p o p u l a t i o n a l o n e . A s time g o e s on t h e r a t i o e x p r e s s e d by przmary productzon/total b i o m a s s drops, both by i n c r e a s e of b i o m a s s a n d by r e d u c t i o n of primary production. D i v e r s i t y i n c r e a s e s a t e v e r y l e v e l . Maturity i n c r e a s e s . T h i s i s s u c c e s s i o n . P e r h a p s t h e m o s t i n s t r u c t i v e period i n t h e e x p e r i m e n t i s when maturity d e c r e a s e s rapidly. Why d o e s d i v e r s i t y d e c r e a s e , a s e n e r g y flow p e r unit b i o m a s s b e c o m e s higher a n d h i g h e r ? A t t h i s moment, t h e s y s t e m i s s u d d e n l y a b l e t o p r o d u c e a g r e a t power o u t p u t , b u t o n l y if t h e r e i s not too much c o n c e r n for e f f i c i e n c y (Odum a n d P i n k e r t o n , 1955). C e r t a i n p i g m e n t s c a p a b l e of rapid s y n t h e s i s a n d o c c u p y i n g a k e y p o s i t i o n i n p h o t o s y n t h e s i s (for e x a m p l e , chlorophyll A) i n c r e a s e much more t h a n o t h e r s . P i g m e n t div e r s i t y d r o p s . Similarly, s p e c i e s with t h e h i g h e s t maximal r a t e of p o t e n t i a l i n c r e a s e b e c o m e a d v a n t a g e o u s l y dominant, a n d d i v e r s i t y drops. We a r e a l w a y s confronted with a f a l l i n s p e c i e s d i v e r s i t y i n s i m i l a r s i t u a t i o n s i n v o l v i n g u t i l i z a t i o n of a s u d d e n b u r s t of p o t e n t i a l productivity, for e x a m p l e , i n a p l a n k t o n bloom, i n a p o l l u t e d river, or i n a c u l t i v a t e d f i e l d . I t s e e m s s a f e t o a s s u m e t h a t maturity h a s a d o u b l e m e a s u r e : In i t s s t r u c t u r a l a s p e c t , it c a n b e m e a s u r e d i n t e r m s of d i v e r s i t y or of complexity

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over a certain number of l e v e l s . In t h e a s p e c t s relating to matter and energy, i t c a n b e measured a s primary production per unit of total biomass. T h e connections between complementary a s p e c t s and measures require theoretical consideration. T h e ratio-primary production/total biomass h a s not been s e l e c t e d for theoretical considerations, but simply b e c a u s e i t is e a s i l y a t hand. But t h e true meaning of biomass, if we think over t h i s expression, h a s to b e construed a s something that is the keeper of organization, something t h a t is proportional to the influence that an actual ecosystem can exert on future events. If t h i s influence over the future i s simply equated with dry weight or any other u s u a l expression of biomass, o n e f o r e s e e s i n a c c u r a c i e s . In f a c t , the s a m e amount of dry weight may have a different influence on future developments according to how i t i s organized. Moreover, elements that actually a r e not counted a s p a r t s of biomass, s u c h as dead wood, burrows, and t h e l i k e , a r e elements of organization, s i n c e they exert a certain influence on t h e future development of t h e ecosystem. From a general theoretical standpoint, i t would be a d v i s a b l e to replace the ratio primary production/total biomass by a more s o p h i s t i c a t e d ratio; turning to t h e conv e r s e (B/P), i t could be defined a s the amount of information that can b e maintained with a definite spending of potential energy. Here information is taken in t h e s e n s e of something a t which l i f e h a s arrived through a s e r i e s of d e c i s i o n s , and that i n f l u e n c e s , in one or another s e n s e , future events. The ratio P / B may be considered a l s o a s metabolism per unit biom a s s . The r a t e of change of a v e r a g e community metabolism i s a l w a y s negative along s u c c e s s i o n . T h e i d e a s developed s o far can be summarized a s follows. An ecosystem that h a s a complex structure, rich in information, needs a lower amount of energy for maintaining s u c h structure. If we consider the interrelations between t h e elements of an ecosystem a s communication c h a n n e l s , we c a n s t a t e that s u c h channels function on the average more effectively, with a lower n o i s e l e v e l , if they are multiple and diverse, linking elements not s u b j e c t e d to g r e a t changes. Then, l o s s of energy i s lower, and t h e energy n e c e s s a r y for preventing decay of the whole ecosystem amounts relatively to l e s s . T h i s s e e m s to be one of the b a s i c principles of ecology, probably recognized tacitly by most writers, although rarely put in an explicit way.
SUCCESSIOK AND FLUCTUATIONS

Any ecosystem not s u b j e c t e d to strong disturbances coming from outside, c h a n g e s in a progressive and directional way. We s a y t h a t t h e ecosystem becomes more mature. T h e two most noticeable c h a n g e s accompanying t h i s p r o c e s s are the i n c r e a s e of complexity of structure and t h e d e c r e a s e of t h e energy flow per unit biomass. T h i s theoretical background l e a d s u s to a c c e p t a sort of natural selection in the p o s s i b l e rearrangements of t h e ecosystem: L i n k s between the elements of an ecosystem c a n be substituted by other l i n k s that work with a higher efficiency, requiring a change in the e l e ments and often an i n c r e a s e in t h e number of elements and connections. T h e new situation now h a s an e x c e s s of potential energy. T h i s c a n b e

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u s e d in developing the ecosystem further, for i n s t a n c e , by adding biomass after driving more matter into the system. A more complex s t a t e , with a reduced w a s t e of energy, a l l o w s maintenance of t h e s a m e biomass with a lower supply of energy-or a higher biomass with t h e s a m e supply of energy - and r e p l a c e s automatically any previous s t a t e . T h e only limit s e t to t h i s progressive change is interference from t h e p h y s i c a l environment. S u c c e s s i o n can build history only when t h e environment is stable. In the c a s e of a changing environment, the s e l e c t e d e c o s y s t e m will be composed of s p e c i e s with a high reproductive rate and lower s p e c i a l requirements. Such a n ecosystem is l e s s diverse and l e s s complex; t h e energy flow per unit biomass remains relatively high. There is another situation where an ecosystem cannot i n c r e a s e maturity: when there is a c o n s t a n t l o s s of individuals by diffusion, sedimentation or exploitation by t h e action of external agents. In s u c h s i t u a t i o n s , something is exported which otherwise could b e u s e d in increasing organization. T h e study of s u c c e s s i o n d o e s not include a l l relations of e c o s y s t e m s with time. In a more refined consideration of c o n c e p t s , diversity may b e represented as the width of a communication channel, a p t to carry along time a certain amount of organization or of information a t t h e s e l e c t e d l e v e l . T h i s s e t s limitations, of course. An ecosystem with a low biotic diversity cannot carry a high degree of true organization. But a highly diversified community h a s t h e capacity for carrying a high amount of organization or information. T h i s does not signify that the potential amount is a l w a y s actually carried. T h e difference c a n be illustrated by comparing a planktonic community with a bottom community over rocky substratum. Both communities may have similar d i v e r s i t i e s , but the organization b a s e d on s u c h ' diversity can b e carried more effectively along time in t h e benthic community. Here, s p a t i a l distribution of individuals belonging to different s p e c i e s (pattern) is preserved, and with i t most of t h e relations e x i s t i n g between s u c h individuals. If we determine t h e pattern of s u c h a community a t a time a, and then a t a subsequent time b, and s o on, we discover that t r a n s i t i o n s from o n e s t a t e to the next follow a notable regularity; the patt e r n ' s deterministic component i s more important than i t s random component. In other words, diversity effectively m e a s u r e s information that is carried along with time. T t h e c a s e of the plankton community, t h e matrix n describing the transition probabilities between s u c c e s s i v e s t a t e s c a n b e recognized a s p o s s e s s i n g a deterministic part and a random part; but here t h e s e c o n d part is more important than in the benthos: think only of t h e turbulence of water, carrying organisms and influencing c o n t a c t s between org a n i s m s of different s p e c i e s . In t h i s situation, t h e channel w i d t t is not effectively u s e d because of turbulence-a random element of t h e environment. P e r h a p s the following analogy may clarify the difference under d i s c u s sion: L e t u s imagine t h e structure of a community in terms of a m e s s a g e , written in a language with a number of symbols equal to the number of s p e c i e s , and where individual symbols s t a n d for individuals. A benthic com-

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munity would b e more l i k e a real text written with t h i s language; a planktonic community would b e rather comparable with an imaginary text in which l e t t e r s were not fixed, but a r e s u b j e c t e d to a certain s o r t of thermic agitation that m a k e s them change p l a c e s over and over again, s o that the amount of information actually carried would be reduced. T h e conclusion i s that in any e s t i m a t e of maturity, not only diversity, but a l s o predictability of change with time h a s to be considered. Ordinarily both c h a r a c t e r s a r e correlated. L e s s mature e c o s y s t e m s not only h a v e a lower diversity, but i n them transition between s u c c e s s i v e s t a t e s i n c l u d e s a higher amount of uncertainty. And more diverse e c o s y s t e m s have, in general, more predictable future s t a t e s . In other words, in more mature e c o s y s t e m s the future s i t u a tion i s more dependent on the present than i t is on inputs coming from outs i d e . q o m e o s t a t i s is higher. On the other hand, future s t a t e s in l e s s mature e c o s y s t e m s a r e heavily influenced by external inputs, by changes in t h e p h y s i c a l environment. L e t u s consider any structure formed by interconnected elements, like a nervous net, an automaton, o r an e c o s y s t e m , a n d s u b j e c t e d to inputs (changes in the p h y s i c a l environment, a s stimuli) and giving off outputs (reaction on t h e environment, population w a v e s , migrations, rhythms of a c tivity and s o on). Internal organization of s u c h a s y s t e m can turn random inputs or disturbances into much more regular outputs or rhythms. C o l e (1951) and Palmgren (1949), among other e c o l o g i s t s , have d i s c u s s e d t h e possibility t h a t "regular" c y c l e s in populations may originate by t h e interaction of random inputs, for example, relative strength of year c l a s s e s , a s related to random c h a n g e s in climatic factors or to alteration in t h e structure of the existing unispecific population and of the whole ecosystem in which t h e population is integrated. T h e properties a s s o c i a t e d with t h e structure of the ecosystem define t h e operations to do with the random inp u t s , and give more o r l e s s regular output patterns. Analogously, a crystalline body converts a random x-ray input into a regular diffraction pattern. I t may b e pertinent for the e c o l o g i s t s to remember here the importance of general t h e o r i e s on automata and nerve n e t s , and t h e theory of storage (Moran, 1959), a n d the recent developments on random theory (Wiener, 1958; s e e a l s o Barlow, 1961). In general, t h e expected differences in t h e character of fluctuations i n l e s s mature and more mature communities would be a s follows. In l e s s mature communities, environmental fluctuations a r e strong and a b l e to s t o p the trend to i n c r e a s e maturity a t a certain level. Maturity does not i n c r e a s e b e c a u s e abiotic fluctuations a r e too strong, and homeostatis i s difficult to attain in a poorly organized, often a pioneer community. In a more s t a b l e environment, s u c c e s s i o n proceeds and maturity i n c r e a s e s ; now w e have to e x p e c t rhythms that are more regular, more independent of environment and often endogenous. Anticipatory power h a s survival v a l u e and is t h e express i o n of a complex s y s t e m , a b l e to produce very efficient homeostatic mechanisms. Up to a certain l e v e l , t h e s e homeostatic mechanisms c a n protect t h e system from disruption due to external a g e n t s . Maturity i s selfpreserving.

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F l u c t u a t i o n s of unispecific populations can b e considered on :he same background. L a r g e fluctuations in populations are to b e e x p e c t e d in l e s s mature e c o s y s t e m s : a rapid i n c r e a s e of numbers of a plant or an animal is p o s s i b l e only i n a system that works with low efficiency, t h e s u b s e q u e n t drop in t h e number of individuals means either a great mortality and consumption by other organisms, or d i s p e r s a l or migration out of t h e e c o s y s tem, in any c a s e a strong flow or export of potential energy. In t h i s s e n s e strong fluctuations in plankton populations represent a heavy export towards other communities, for i n s t a n c e , towards t h e benthos. Planktonic communities retain always a l e s s mature character than benthic communit i e s , and i t i s to be expected, in good agreement with observation, t h a t fluctuations in planktonic populations a r e of shorter period and wider ranges. Fluctuations of an e c o s y s t e m often may b e considered a s fluctuations in t h e degree of maturity around an average maturity. At certain periods of t h e year t h e ecosystem i s l e s s mature than a t other times. Such c h a n g e s could b e considered a s true s u c c e s s i o n s , starting again and again. In t h e plankton, for i n s t a n c e , the period of vertical mixing of water corresponds to a l e s s mature a s p e c t of the whole ecosystem and can b e taken a s t h e starting point of a s u c c e s s i o n of phytoplankton. In other elements of pel a g i c life, c h a n g e s a r e simple fluctuations, rather than true s u c c e s s i o n s . T h e n e c e s s a r y energy to disrupt an ecosystem probably maintains certain relations with t h e attained maturity. Anything that k e e p s an ecosystem o s c i l l a t i n g , retains i t in a s t a t e of low maturity. Often i t i s t h e environment, a s in the c a s e of s u c c e s s i o n s of phytoplankton. At other times i t is an a c tive exploitation from outside that forces a repeated reconstruction and a n output of work reconcilable only with l e s s mature s t a t e s . B e c a u s e i t is of practical value, I want to s t a t e again that fluctuations in l e s s mature s y s t e m s are more related to environmental c h a n g e s , to abiotic factors; but fluctuations in more mature e c o s y s t e m s a r e more dependent on internal conditions of equilibrium, that i s , on biotic factors. Fluctuations in the populations are, of course, accompanied by fluctuations in t h e biotically controlled properties of environment. For i n s t a n c e , strong yearly fluctuations in the phosphate content of water are linked to l e s s mature and strongly fluctuating plankton populations. T h e y are related a l s o to e s s e n t i a l l y exploitable fish populations, a s Cushing remarked, that i s , to fish populations c a p a b l e of great changes in numbers and, thus, c a pable of supporting human extraction. In t h e more mature e c o s y s t e m s , with damped fluctuations, t h e supply of nutrients in t h e environment i s k e p t constantly a t a low level, a s in tropical f o r e s t s .
EXTENSIVE SYSTEhlS WITH LOCAL DIFFERENCES IN THE VALUE O F VATURITY

Ue can m e a s u r e a global property of e c o s y s t e m s - named maturity for C ' convenience - i n different ways: in terms of structure and in terms of energy flow per unit biomass. Applying t h e s e criteria in t h e a n a l y s i s of t h e parts of any extensive system, i t is p o s s i b l e to e s t i m a t e maturity in t h e different points, and map t h e v a l u e s , s a y , of s p e c i e s diversity, of pigment

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diversity, of primary production per unit of total biomass. A s i s to b e expected, the different maps s o prepared are congruent (Margalef, 1961b; Herrera, Margalef and Vives, in p r e s s ) and, in general, i t is p o s s i b l e to t r a c e s u r f a c e s linking a l l the points that h a v e a similar degree of maturity. Every o n e of s u c h s u r f a c e s i s a boundary between a subsystem of lower maturity and a subsystem of higher maturity. We c a n repeat s u c h maps a t different times, in order to study s u c c e s s i o n and c h a n g e s in t h e general pattern of distribution of maturity. A s is well known, s u c c e s s i o n and s p a t i a l heterogeneity a r e strongly linked (Margalef, 1758). Heterogeneity often originates b e c a u s e s u c c e s s i o n proceeds a t different s p e e d s according to t h e location, and i t is a common experience of e c o l o g i s t s that e n c l a v e s or s p o t s with a lower maturity -immersed i n more mature s y s t e m s - a r e related to some l o c a l disturbance (strong mixing by underwater springs in the s e a , p r e s e n c e of bare rock in terrestrial vegetation, etc.). T h e s e exclude, a t l e a s t for t h e moment, a further progress in t h e s u c c e s s i o n . Every reader will remember s k e t c h e s in t r e a t i s e s on ecology depicting t h e vegetation g i r d l e s around a s e n e s c e n t l a k e and showing differences in maturity, that i s , in t h e s t a g e reached i n s u c c e s s i o n if w e a s s u m e a general trend towards increasing maturity. lvlaps depicting the distribution of biotic diversity, and of t h e ratio D,,,/D,,, (optical d e n s i t i e s a t t h e s t a t e d wavelengths of a c e t o n e e x t r a c t s ) i n plankton populations, are of t h e same kind. T h i s ratio is a simplified expression of t h e diversity of pigments. The distribution of t h e v a l u e s of t h e ratio primary production/respiration, u s e d by H. T . Odum, may have a similar meaning. L e t u s explore what happens along a s u r f a c e of equal maturity. Remember that a t one s i d e w e have a subsystem of lower maturity, with a high production per unit biomass, with l e s s strong l i n k s between s p e c i e s , subject to wider fluctuations and to an e a s y d i s p e r s a l of the elements. At t h e other s i d e we find a subsystem with a greater biomass for t h e s a m e energy flow, with well organized relations over elements more strongly localized. If maturity i n c r e a s e s i n the l e s s mature system, e s p e c i a l l y a t the proximity of t h e boundary (which i s to b e e x p e c t e d from s u c c e s s i o n ) the s u r f a c e of equal maturity moves towards t h e l e s s mature subsystem. T h i s i s probably accompanied by a flow of energy going the converse way. T h i s means that matter (biomass and non-living matter) goes in both directions, s i n c e both coupled s u b s y s t e m s a r e actually open, but t h e content of potential energy of s u c h matter i s , on the average, higher in t h e matter going the way of increasing maturity than in the matter going the way of d e c r e a s i n g maturity. T h e subsystem with a lower maturity maintains a higher ratio between primary production and total p r e s e n t biomass, b e c a u s e i t actually l o s e s biomass, in going a c r o s s the border to the more mature coupled subsystems. L e t u s remember that s u c c e s s i o n is simply t h e exchange of an e x c e s s a v a i l a b l e energy in the present, for a future i n c r e a s e of biomass. An ecos y s t e m i n i t s present s t a t e i s l e s s mature a n d h a s an e x c e s s production that g o e s to t h e future and h e l p s reorganize t h e ecosystem in a more mature

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form. If there i s no a v a i l a b l e e x c e s s production or i t is drained out of the s y s t e m , s u c c e s s i o n proceeds no further. We will find no difficulty in applyi n g t h e s a m e type of relation, not to s u c c e s s i v e s t a t e s of t h e s a m e s y s t e m , but to adjoining s y s t e m s . What t h e one d o e s in e x c e s s (production) i s put i n u s e by t h e other. There i s a transfer, or an exchange, between energy and what can be called an "organizing influence." It s e e m s important to s t r e s s that t h e different degrees of maturity of two coupled s u b s y s t e m s c a n be, and have to be, estimated through t h e study of structure and turnover of every subsystem, with total independence of t h e eventual e x i s t e n c e and direction of any exchange between both s u b s y s t e m s . In other words, i t is not n e c e s s a r y to find out that there is a certain exchange between s u b s y s t e m s , in order to l a b e l automatically a s t h e l e s s mature t h e subsystem that exports, and a s the more mature t h e importing subsystem. T h e d i s c u s s i o n of some concrete examples will permit t h e development of t h e s e i d e a s , and the proper consideration of changing properties along t h e boundary. Intensity of exchange between s u b s y s t e m s of different maturity may b e quite different. Plankton, in general, i s a l e s s mature system than the benthos. All t h e required qualifications a r e there: lower s p e c i e s diversity, lower pigment diversity (lower ratio D,,,/D,,,), more uncertainty in defining t h e relations between s u c c e s s i v e s t a t e s and higher primary production per unit of t o t a l biomass. In t h e coupling of plankton and benthos, a net transfer of energy e x i s t s from plankton to benthos; i t can be s a i d that the plankton, in part, f e e d s the benthos. Such exchange i s due to the combination of s e v e r a l eff e c t s . There i s a major p a s s i v e factor: sedimentation of plankton. There a r e other, biotic, factors, s u c h a s the e x i s t e n c e of benthonic filter-feeders that actively attract t h e plankton, pumping production from plankton to benthos. T h e r e a r e a l s o benthonic animals t h a t produce planktonic larvae. L a t e r t h e s e larvae become a d u l t s and return to t h e benthonic environment. In general, potential energy going towards t h e benthos in the form of t h e s e t t l i n g larvae is higher than potential energy going t h e opposite way in t h e form of reproductive c e l l s or hatched larvae. It is worthwhile to d i s c u s s further t h e relative and the combined import a n c e of t h e s e effects. An a c t i v e exploitation by t h e more mature s y s t e m may prevent the progressive development of a coupled subsystem, keeping i t in a s t a t e of low maturity. A s an example, we may c i t e the heavy p a s s i v e l o s s resulting from t h e sedimentation of plankton. T h e fact i s that t h e prese n c e of bottom filter-feeding animals in an aquarium drives the free-floating population into a s t a t e of lower maturity. Also, animals harboring symbiotic a l g a e probably maintain them in a s t a t e of lower maturity, through a c t i v e absorption of organic compounds. Looking for an analogy in human affairs we may compare s u c h a coupling to colonialism: a master country, taking out t h e product of an underdeveloped country, impedes i t s economic progr e s s ; that i s , i t s maturity T h e s t e e p n e s s of the gradient between a more mature and a l e s s mature subsystem d e p e n d s not only on a c t i v e exploitation, but a l s o on other char-

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a c t e r i s t i c s . Light is a b a s i c factor i n plankton production and i s more i n t e n s e above. Furthermore, sedimentation l e a d s a part of t h e produced biomass down. It is t h u s natural to e x p e c t t h a t s u r f a c e planktonic populations will b e , in general, l e s s mature than populations living a t greater depths. T h e contrast may be enhanced a t t h e l e v e l of pycnoclines; the s t e e p n e s s of gradients is particularly sharp where there i s a reduced rate of diffusion or exchange. In s u c h a c a s e , the intensity of exchange between coupled s u b s y s t e m s i s clearly related to environmental variables. The i d e a s developed in the p r e s e n t s e c t i o n a r e e a s i l y t e s t a b l e by coupling two culture v e s s e l s containing populations of different maturity. One culture c a n be maintained in a situation of lower maturity by being continuously stirred. In t h i s one we will have a bloom of small c e l l s . In the other container, w e observe, in most replications of t h e experience, a notable development of swimming organisms, a heavy growth over t h e w a l l s and a more important proportion of animal life. T h i s i s a simple s c h o o l experiment, but i t i l l u s t r a t e s how net energy-flow g o e s from the l e s s towards t h e more mature, that i s , towards the unstirred subsystem. T h i s experiment c a n be performed by placing t h e containers s i d e by s i d e , a t t h e s a m e l e v e l , with a connecting tube; a l s o in t a l l , stratified v e s s e l s , where i t proves that sedimentation in plankton is o n e of the multiple mechanisms of transfer. If we want to consider a comparable example in terrestrial ecology, perh a p s we could t a k e t h e boundary between a forest and a p l a c e with open and low vegetation. T h e boundary should h a v e a tendency to be d i s p l a c e d towards t h e open land; i t i s expected that there will b e more animals in t h e forest getting food from g r a s s l a n d , than animals in the g r a s s l a n d getting food in the forest.
CONTRACTION AND EXPANSION O F THE ECOSYSTEhl

In vagrant communities, like plankton, subsidiary problems appear. Here we must choose, a s reference, between a system of coordinates fixed i n s p a c e o r a s e t of coordinates moving with the populations or with t h e water m a s s e s . When transport is accompanied by deformation, if t r a j e c t o r i e s a r e not parallel and have different s p e e d s , problems become increasingly complex. T h e r e i s a possibility that some of t h e s e problems a r e not without a n a l o g i e s i n physics. Expansion of e c o s y s t e m s in s p a c e i s frequently a s s o c i a t e d with individual trajectories a t random, and means a reduction in maturity. In contracting communities, movements a r e often organized and l e a d to an i n c r e a s e of maturity, or a t l e a s t of diversity per unit s p a c e . T h e s e p r o c e s s e s a r e perhaps not absolutely general, but may be followed e a s i l y in laboratory cultures p l a c e d in appropriate experimental conditions. T a k e , for i n s t a n c e , cultures in a liquid medium p l a c e d in containers s e p a rated by a g l a s s filter-barrier, with the possibility of pumping medium a c r o s s the porous wall. We can obtain, a t will, the u s u a l drop of diversity and i n c r e a s e in t h e primary production per unit biomass in the subculture towards which we pump t h e fluid. Another good example, t h i s one in nature, i s afforded by the behavior and distribution of plankton in a s y s t e m formed

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by alternating convergences and divergences, or convection c e l l s . T h e divergences harbor l e s s mature and expanding populations, with many diatoms, low diversity, etc., while i n the convergences a r e found communities of a more mature character; they a r e contracting b e c a u s e f l a g e l l a t e s k e e p moving or swimming upwards to become concentrated above. T h e whole structure b e h a v e s a s the coupling of l e s s mature (divergence) with more mature (convergence) s u b s y s t e m s , with t h e expected net transfer of production from t h e divergences to the convergences. Sedimentation of p a s s i v e plankton i s another illustration of the s a m e general model, where transport is directed downwards. In t h e upper l a y e r s , plankton becomes diluted or d i s p e r s e d and in t h e lower l e v e l s i t is concentrated. T h e continuous drain of a part of the s u r f a c e plankton n e e d s to be countered by an e x c e s s production and d o e s not allow a g r e a t i n c r e a s e in organization. For t h i s reason, plankton remains l e s s mature in the upper l e v e l s and other e f f e c t s (exploitation, active movements) may make t h i s vertical difference more conspicuous, or change i t otherwise. Other similar models, where the horizontal dimensions are more important, c a n be constructed to represent populations in e s t u a r i e s (both normal or positive, and hypersaline or negative) and a l s o to represent running wat e r s in general, in which the i n c r e a s e in maturity i s always downstream (Margalef, 1960). One need i s for the mathematical t o o l s n e c e s s a r y to compute the movements, or the relative displacements, of elements in an ecosystem in terms of any s u i t a b l e measure of structure. If t h i s is achieved, t h e way i s open for adding the e f f e c t s of transport and s u c c e s s i o n , e x p r e s s i n g the r e s u l t s a s c h a n g e s in maturity. Such a possibility would be useful in dealing with planktonic communities.
T H E PARTITION O F UNISPECIFIC POPULATIONS hlOVING F R E E L Y ACROSS
ECOSYSTEhlS WITH LOCAL D I F F E R E N C E S IN MATURITY

Any unispecific population that expands over a wide range h a s l o c a l diff e r e n c e s in t h e demographic structure, even when internal flow of individu a l s i s important. Any portion of t h e population with a higher proportion of young individuals (suggesting a lower average l i f e s p a n , and a higher mortality) means a higher energy-flow per unit of biomass. By an obvious analogy, t h e population c a n be s a i d to h a v e a l e s s mature demographic structure. In the p l a c e s where s u c h populations e x i s t , fluctuations a r e shorter and t h e range in change of biomass i s wider. Broadly speaking, there is a s p a t i a l correspondence between t h e localization of the l e s s mature portion of a unispecific population and t h e l e s s mature parts of the whole system. Good examples a r e furnished by benthic animals that send larvae and young to the l e s s mature and superficial wat e r s , and by migrating birds breeding in the l e s s mature e c o s y s t e m s of temperate latitudes. Animals tend to s p e n d their a d u l t l i v e s in t h e more mature s y s t e m s , but to reproduce in t h e l e s s mature o n e s and s e n d larvae or reproductive elements into them.

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Monte Lloyd, in a personal communication d i s c u s s i n g t h i s point, exp r e s s e d i t s meaning very clearly: "I tend to s e e t h i s a s a reflection of a previous evolutionary history: i t h a s always been an advantage to reprod u c e on l e s s mature e c o s y s t e m s , s i n c e t h e s e a r e maintaining t h e m s e l v e s l e s s efficiently, and energy needed for growth i s more readily available. Competition for i t i s l e s s s e v e r e . T h o s e individuals t h a t developed behavior p a t t e r n s which led them to reproduce in l e s s mature s y s t e m s h a v e l e f t behind more offspring. They h a v e been s e l e c t e d for. T h e a d u l t s , which live in more mature e c o s y s t e m s s e n d their young o u t s i d e to l e s s mature s y s t e m s to gather energy (growth) and bring i t back. Here, certainly is a 'directive influence' emanating from the more mature e c o s y s t e m s . " In the Mediterranean c o a s t s of E a s t Spain a very good example h a s been worked out. From the mouth of the Ebro River towards t h e South, there is a gradient of increasing maturity in the planktonic ecosystem. It i s well reflected in diversity i n d i c e s , pigment composition and other properties. There is an important breeding a r e a of s a r d i n e i n the l e s s mature part of the system, and t h e demographical structure of t h e f i s h populations c h a n g e s gradually a s maturity of the ecosystem in which they a r e incorporated inc r e a s e s (data of M. Gomez Larraneta and coworkers). Human exploitation, if restricted geographically, l e a d s to a l o c a l d e c r e a s e of maturity, both of t h e general ecosystem and in the demographical structure of t h e s e l e c t i v e l y exploited s p e c i e s . Many other examples could be found in i n s e c t s that breed in aquatic environments but have adult forms that a r e integrated into terrestrial e c o s y s tems, or in fish that breed in inundation waters. The f i s h that migrate between s e a water and fresh water offer a s p e c i a l s u b j e c t for meditation. E e l s breed in the s e a and s p e n d their adult life in fresh water; in salmon t h e converse i s true. How c a n t h i s be made c o n s i s t e n t with our theory that requires animals to breed always in the l e s s mature part of t h e a v a i l a b l e s y s t e m s ? E e l s develop in the marine pelagic environment, one of the l e a s t mature of marine e c o s y s t e m s . Adult e e l s belong to t h e bottom of lowland fresh water, a relatively mature system. Salmon breed in t h e upper s t r e t c h e s of streams, one of the l e s s mature fresh-water e c o s y s t e m s . Adult salmon, on t h e contrary, belong to a more mature system i n the marine littoral. A similar parallelism or adjustment between demographic or a g e structure and general maturity of the e c o s y s t e m is observed not only a c r o s s s p a c e , but a l s o along time. Planktonic animals with a regular reproductive c y c l e breed when t h e whole mixed population i s i n a l e s s mature s t a t e , after a pulse of primary production, and when an important surplus of food i s available. In t h i s moment the demographic structure of t h e s p e c i e s under consideration i s in a s t a t e of very low "maturity."
T E M P E R A T U R E AND MATURITY

A higher temperature i n d u c e s a higher flow of energy ( i n c r e a s e d respiration) per unit biomass; organisms are a l s o smaller and h a v e a shorter life

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span. T h e s e c h a n g e s , observed in the populations of a s p e c i e s a t different temperatures, l e a d s u s to predict a certain relation between high temperature and low maturity. T h i s parallelism s e e m s to b e reinforced by other coincidences. An e c o s y s t e m h a s c h a n c e s of survival with different d e g r e e s of organization, that i s , with higher or with lower maturity. But the general trend i s towards an i n c r e a s e of maturity. T h e r e a s o n s for t h i s may h a v e to do with certain principles of thermodynamics. Something similar h a p p e n s in temperature relationships. T h e r e a r e organisms well adapted to high temperature and to low temperature, but t h e more common trend in evolution s e e m s to b e towards t h e production of organisms b e t t e r f i t for a lower temperature- bigger s i z e , longer life, and s o on (Margalef, 1955). Here is a suggestion, a l s o , of the operation of very general p h y s i c a l principles. But t h e ecological picture i s rather diverse. At p r e s e n t and i n our planet, t h e most mature e c o s y s t e m s , t h e coral reef in the s e a , t h e tropical f o r e s t on land, a r e restricted to warmer environments. In my opinion t h i s i s not related to temperature, but to stability of environment. A s t a b l e environment, warm or cold, a l l o w s t h e i n c r e a s e of maturity u p to a l e v e l much higher than a fluctuating environment, cold or warm. Coral reefs a r e a good example of very mature e c o s y s t e m s limited to a r e a s of g r e a t s t a b i l i t y , rather than to a r e a s of a definite temperature a s i s generally believed. They a r e lacking in many tropical w a t e r s where yearly fluctuations in phosphate content, for i n s t a n c e , a r e important. Indeed, in s u c h a r e a s with fluctuating conditions (north-east of Venezuela, for i n s t a n c e ) , we h a v e important p u l s e s of phytoplankton, accompanied by a heavy development of clupeids, a l l indicators of much l e s s mature e c o s y s t e m s .
MATURITY AND EVOLUTION

A related problem that I h a v e d i s c u s s e d elsewhere (Margalef, 1958, 1959) i s t h e relation between pattern (rhythm and mode) of evolution and maturity of t h e ecosystem in which the s p e c i e s evolves. In l e s s mature e c o s y s t e m s or in l e s s mature trophic l e v e l s of a n y ecosystem, we expect s p e c i e s to b e short-lived, e a s i l y d i s p e r s e d , a b l e to colonize with rapidity virgin a r e a s , a b l e to l e a v e numerous offspring and, Phenotypes of course, characterized by high ratio energy flow/biomass. may b e p l a s t i c , cyclomorphosis or temporary variation is common, and genetic compatibility between s e p a r a t e and d i s t a n t populations i s rarely l o s t . They a r e euryoic, competition is for dominance and evolution may be rapid. They are opportunistic s p e c i e s , s u b j e c t e d to a dynamic type of s e l e c t i o n , often for prolificness. In more mature e c o s y s t e m s or in more mature a r e a s of their structure, the s e l e c t e d s p e c i e s a r e of rather long life, with limited but well protected offspring, and with more r e s t r i c t e d p o s s i b i l i t i e s of dispersion accompanied by isolation in small breeding units. T h e s p e c i e s a r e very well integrated in the r e s p e c t i v e e c o s y s t e m s from the standpoint of biochemistry, nutritional n e e d s , behavior, and s o on. They h a v e well developed territorial i n s t i n c t s ,

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endogenous rhythms, e t c . Development is often c a n a l i z e d and morphologic a l stability is high, but g e n e t i c differences between the diverse breeding u n i t s a r e common. Competition between c l o s e l y related forms may become limited. S u c c e s s is linked to efficiency and manifested in a stabilizing type of s e l e c t i o n . No wonder evolution in l e s s mature e c o s y s t e m s , implying a higher flow of energy per unit biomass, is more expensive and by t h i s very f a c t can b e more creative or, a t l e a s t , go faster. Another point i n the relation between maturity and evolution i s worth to recall. By t h e f a c t of s u c c e s s i o n , conditions of equilibrium in every e c o s y s tem are slowly shifting towards c h a r a c t e r i s t i c s of i n c r e a s e d maturity, and the evolution of s p e c i e s i s "sucked" towards a better adjustment to conditions of ever-increasing maturity. In the slow p r o c e s s of evolution, s o w e l l manifested in the f o s s i l record of phylogenetic s e r i e s , we can expect many s e r i e s demonstrating an adjustment to conditions of increasing maturity of e c o s y s t e m s .
UTILITY O F A SYNTHETIC APPROACH

Most of what h a s been d i s c u s s e d can b e summarized in two very simple principles: (1) T h e relative amount of energy n e c e s s a r y for maintaining an e c o s y s tem is related to the degree of structure or organization of t h i s ecosystem. L e s s energy i s n e c e s s a r y for a more complex ecosystem, and the natural trend in s u c c e s s i o n is towards a decreasing flow of energy per unit of biom a s s and towards increasing organization. Briefly s t a t e d the trend i s towards increasing maturity. (2) When two s y s t e m s of different maturity meet along a boundary that allows an exchange, energy (production) flows towards the more mature s u b s y s t e m , and the boundary or surface of equal maturity shows a trend to move i n an opposite direction to s u c h energy flow. T h e s e general principles clarify many ecological interactions and proce s s e s and allow quantitative formulation. They c a n be u s e d or t e s t e d in predicting changes induced by human action. Exploitation is like inflicting a wound upon a heterogeneous organic structure: some t i s s u e s or s u b s y s tems (more mature) do not regenerate; other ( l e s s mature) d o and t h e s e supply the b a s i s for a further eventual i n c r e a s e of maturity. Maintained exploitation k e e p s the maturity of the exploited system constantly low. Exploited natural communities come to have a higher primary production per unit biomass, a lower s p e c i e s diversity and, presumably, a lower ratio More energy g o e s into fluctuations s u c h a s those represented by exploited populations or by populations that a r e integrated into exploited ecosystems. For example, p e s t s have fluctuations with a wider range and shorter periodicity than similar populations that are integrated into more mature, eventually unexploited, e c o s y s t e m s . Extremely mature e c o s y s t e m s , such a s tropical f o r e s t s , a r e unable to go back and a r e totally disrupted by human exploitation. The examples furnished by f i s h e r i e s are illustrative:

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very productive f i s h e r i e s belong to e c o s y s t e m s of low maturity, with a fluctuating supply of inorganic nutrients and with notable p u l s e s in plankton production. T h e l e s s the maturity, the more important the "abiotic" control of populations. Human activity d e c r e a s e s maturity and can enhance fluctuations. T h e notable exclusion between coral reefs and a heavy production of clupeids in tropical waters h a s been c i t e d and i t is p o s s i b l e to hypothesize that pollution and other alterations along tropical c o a s t s may destroy very mature e c o s y s t e m s , and then f i s h e r i e s can become more important than a t present. Radiation i n c r e a s e can b e e x p e c t e d to a c t destructively to accumulated information (that i s , to biomass) but with no effect on potential energy flow; radiation, then, must reduce the maturity of ecos y s t e m s , in part by s e l e c t i v e destruction of the more mature elements of the ecosystem. T h u s , a great i n c r e a s e in radiation may mean a new push given to an already lagging evolution. Most of the same principles c a n be applied to human organizations. Taking a s criteria t h e diversification of s k i l l s and jobs (diversity), or the relat i v e flow of potential energy, i t is p o s s i b l e to map the "maturityJ7 of s t a t e s and continents in the ecological s e n s e of organization. Energy flow g o e s from l e s s mature (rural) a r e a s to more mature (urban) a r e a s . T h e urban cent e r s represent l o c a l i z e d elements that have accumulated high amounts of information, fed on the production of neighboring s u b s y s t e m s , and h a v e exerted a directive actlon, Very old s y s t e m s c a n survive with a small flow o f energy, and l i k e their ecological counterparts can break down a s a cons e q u e n c e of a minor environmental change. It is p o s s i b l e to d e a l objectively and quantitatively with big and complex structures, if one never forg e t s t h e complementary a s p e c t s of energy a s r e l a t e d t o matter, a n d structure.
SUMMARY

An attempt is made to provide some unifying principles in ecology. T h e structure of e c o s y s t e m s is considered in relation to various components, with emphasis on the c h a r a c t e r i s t i c s of maturity a s measured by diversity d a t a and other determinable features, including primary production (P) and biomass (B). E c o s y s t e m s with complex structure a n d containing a high amount of information can b e maintained with a relatively lower expenditure of energy. Oscillations, introduced for example by environmental c h a n g e s or outside exploration, tend to retain an ecosystem i n a s t a t e of lower maturity. Where s u c c e s s i o n is occurring, involving exchange of an e x c e s s of available energy for a future i n c r e a s e in biomass, the relations encountered may b e applied not only to s u c c e s s i v e s t a t e s in the same system, but t o adjoining or coupled s u b s y s t e m s . S t e e p n e s s of t h e gradient between subs y s t e m s is shown to depend on s e v e r a l factors s u b j e c t to quantitative d e termination and t h e relation between t h e s e s u b s y s t e m s c a n be imitated by simple experiment. When e c o s y s t e m s contract or expand there are corresponding i n c r e a s e or d e c r e a s e s of maturity. F a c t o r s affecting t h e maturity of e c o s y s t e m s and of s p e c i a l i n t e r e s t a r e t h e movement of s p e c i e s . T h e s e s u g g e s t a s p a t i a l correspondence between

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the juvenile or immature portion of an unspecific population and the l e s s mature p a r t s of e c o s y s t e m s a v a i l a b l e for habitation. Maturity is related to evolution in a way t h a t permits generalization concerning the type of organisms to b e found i n e c o s y s t e m s of more o r l e s s maturity and stability. As evolution proceeds, there is a trend toward adjustment to maturity. The c o n c e p t s that emerge may be applied to human s o c i a l s y s t e m s . Two principles become evident: The energy required to maintain an ecosystem is inversely related to complexity, with the natural trend toward decreasing flow of energy per unit biomass; that i s , i n c r e a s e d maturity. Secondly, in a d j a c e n t s y s t e m s there is a flow of energy toward the more mature s y s tem and an opposite movement in the boundary or s u r f a c e of equal maturity.
LITERATURE CITED

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