Biological availability of sediment-bound trace metals

More free publications from Archimer La Baie de Seine (GRECO-MANCHE) - Université de Caen, 24-26 avril 1985 IFREMER. Actes de Colloques n. 4 1986, pages 347 à 362 30 BIOLOGICAL AVAILABILITY OF SEDIMENT-BOUND TRACE METALS. LUOMA S.N. * ABSTRACT^ T h e i m p a c t s of trace contaminants in aquatic e n v i r o n m e n t s c a n n o t be a s s e s s e d r e a l i s t i c a l l y w i t h o u t a g r e a t e r u n d e r s t a n d i n g of t h e f a c t o r s c o n t r o l l i n g the biological a v a i l a b i l i t y of t h e c o n c e n t r a t e d p o o l of m e t a l s a s s o c i a t e d w i t h sediments. I t has been e s t a b l i s h e d t h a t d i r e c t uptake of (at l e a s t some) t r a c e m e t a l s from s e d i m e n t s c o n t r i b u t e s t o m e t a l c o n c e n t r a t i o n s in b e n t h i c o r g a n i s m s . I m p o r t a n t c o n t r o l s on m e t a l u p t a k e from s e d i m e n t a r e t h e c o n c e n t r a t i o n o f t h e e x p o s u r e , the p a r t i t i o n i n g o f t h e m e t a l s among c o m p o n e n t s o f t h e s e d i m e n t , and t h e redox p o t e n t i a l of t h e s e d i m e n t . Important problems in e c o l o g y , p h y s i o l o g y , g e o c h e m i s t r y and b i o g e o c h e m i s t r y r e m a i n unresolved, however, and a c o n c e n t r a t e d interdisciplinary r e s e a r c h e f f o r t w i l l be n e c e s s a r y b e f o r e a c o m p l e t e u n d e r s t a n d i n g o f t h e f a t e and i m p a c t o f s e d i m e n t - b o u n d m e t a l s w i l l be p o s s i b l e . INTRODUCTION One important objective of studying trace metal biogeochemistry is to develop means of predicting or understanding the b i o l o g i c a l impact of t h e s e c o n t a m i n a n t s , based upon t h e i r c o n c e n t r a t i o n s i n t h e e n v i r o n m e n t . This w i l l require u n d e r s t a n d i n g b o t h b i o l o g i c a l and g e o c h e m i c a l a s p e c t s o f t r a c e metal behavior. When a m e t a l i s r e l e a s e d i n an a q u a t i c s y s t e m i t i m m e d i a t e l y d i s t r i b u t e s b e t w e e n p a r t i c l e s and s o l u t i o n . C o n c e n t r a t i o n s bound t o p a r t i c l e s ( s e d i m e n t s or s u s p e n d e d p a r t i c u l a t e s ) a r e u s u a l l y o r d e r s of m a g n i t u d e h i g h e r than c o n c e n t r a t i o n s in s o l u t i o n . This p a p e r i s a summary o f some o f t h e work we h a v e done s t u d y i n g t h e p r o c e s s e s t h a t d e t e r m i n e t h e e x t e n t o f t r a n s f e r t o f o o d webs o f metals within this concentrated p a r t i c u l a t e - a s s o c i a t e d metal reservoir. *U. S. G e o l o g i c a l S u r v e y , M a i l S t o p Menlo P a r k , C a l i f o r n i a 9 4 0 2 5 , USA 465, 345 Middlefield Road, 348 1. SEDIMENT GEOCHEMISTRy OF METALS P a r t i c l e s i n e s t u a r i n e e n v i r o n m e n t s a r e c o m p o s e d o f a number of c o m p o n e n t s c a p a b l e of s t r o n g l y b i n d i n g t r a c e m e t a l s . In o x i d i z e d s e d i m e n t s ( w h i c h w i l l be c o n s i d e r e d e x c l u s i v e l y i n t h i s paper) t h e s e i n c l u d e o x i d e s of i r o n , o x i d e s of manganese, v a r i o u s f o r m s o f o r g a n i c m e t a l s and c l a y s . Most p a r t i c l e s a r e a g g r e g a t e s of a l l t h e s e components (Jenne 1 9 7 7 ) . Most of t h e o r g a n i c m a t e r i a l s , i r o n o x i d e s and m a n g a n e s e o x i d e s o c c u r a s c o a t i n g s often covering clay surfaces. By t h e m s e l v e s , c l a y s a l s o b i n d m e t a l s l e s s s t r o n g l y than the other components ( D a v i e s - C o l l e y e t al 1985). The c o m b i n a t i o n o f a l o w e r b i n d i n g i n t e n s i t y a n d a l o s s of b i n d i n g s i t e s to i n t e r a c t i o n s w i t h o t h e r components s u g g e s t s c l a y s a r e much l e s s i m p o r t a n t t h a n o t h e r t y p e s o f components in b i n d i n g m e t a l s in s e d i m e n t s (Jenne, 1977, D a v i s Colley et al., 1984). The d i s t r i b u t i o n o f a m e t a l among t h e c o m p o n e n t s o f t h e s e d i m e n t s i s d e t e r m i n e d by t h r e e f a c t o r s : ( 1 ) The i n t e n s i t y o f metal binding to each component; (2) t h e number of a v a i l a b l e b i n d i n g s i t e s p e r u n i t mass o f e a c h c o m p o n e n t ; and (3) t h e m a s s o f e a c h component per u n i t mass of s e d i m e n t . By q u a n t i t a t i v e l y c h a r a c t e r i z i n g each of the above a m a t h e m a t i c a l d e s c r i p t i o n of m e t a l d i s t r i b u t i o n w i t h i n a g i v e n s e d i m e n t s h o u l d be p o s s i b l e ( O a k l e y e t a l . , 1 9 8 2 ; Luoma and D a v i s , 1 9 8 3 ; D a v i e s - C o l l e y 1 9 8 4 ; Tessier et a l . , 1984). H o w e v e r , a number o f t h e p r e q u i s i t e s f o r an a c c u r a t e m o d e l a r e p o o r l y k n o w n . Poorly understood factors i n c l u d e (1) m e a s u r e s of b i n d i n g i n t e n s i t y t h a t are c o m p a r a b l e among c o m p o n e n t s ; ( 2 ) t h e e f f e c t o f c o m p o n e n t i n t e r a c t i o n s w i t h i n a g g r e g a t e s upon t h e number o f b i n d i n g s i t e s ; ( 3 ) t h e c o n s t a n c y o f b i n d i n g i n t e n s i t y at d i f f e r e n t metal c o n c e n t r a t i o n s per u n i t c o m p o n e n t ; and ( 4 ) how t o c o n v e r t m e a s u r e s o f component c o n c e n t r a t i o n s t o number o f c o m p o n e n t b i n d i n g s i t e s p e r u n i t mass o f s e d i m e n t (Luoma and D a v i s 198 3 ) . Thus, model c a l c u l a t i o n s of metal p a r t i t i o n i n g ( D a v i s - C o l l e y , et a l , 1984; T e s s i e r , et a l . , 1984, Luoma, in p r e s s ) must be c o n s i d e r e d simplistic approximations. In l i e u of a t e c h n i q u e f o r p r e c i s e l y m o d e l i n g metal p a r t i t i o n i n g in s e d i m e n t s , o p e r a t i o n a l t e c h n i q u e s have been developed. A l a r g e number of l e a c h i n g t e c h n i q u e s h a v e been applied to aquatic sediments (Gibbs, 19 7 3 ; F o r e s t n e r 1979; T e s s i e r , 1979). N e a r l y a l l s u f f e r from a l a c k of chemical s p e c i f i c i t y (Luoma a n d J e n n e , 1 9 7 6 ; G u y , e t a l . , 1 9 7 8 ) ; and f e w , i f a n y , e f f i c i e n t l y e x t r a c t m e t a l from a s i n g l e c o m p o n e n t o f t h e sediment. Statistical techniques a l s o are employed to assess p a r t i t i o n i n g (Luoma and Bryan 1 9 8 1 ) but t h e s e a r e q u a l i t a t i v e and s u b j e c t t o t h e e r r o r s of any c o r r e l a t i v e a p p r o a c h , e s p e c i a l l y those a s s o c i a t e d with confounding v a r i a b l e s . D e s p i t e t h e i r i n a d e q u a c i e s , some c o n s i s t e n t conclus ions e m e r g e from t h e d i f f e r e n t approaches to studying metal partitioning. The c l e a r e s t i s t h a t m o s t m e t a l s d i s t r i b u t e among s e v e r a l c o m p o n e n t s or t y p e s of b i n d i n g s i t e s in o x i d i z e d sediments. I t a l s o a p p e a r s t h a t t h i s d i s t r i b u t i o n can c h a n g e i f the c h e m i c a l c h a r a c t e r i s t i c s of the s e d i m e n t s change. Leaching studies c o n s i s t e n t l y show t h a t s e v e r a l m e t a l f r a c t i o n s of d i f f e r e n t e x t r a c t a b i l i t y o c c u r in a l m o s t a l l s e d i m e n t s . A 349 'ùffilmêHj-M\**à Figure 1 . P a r t i t i o n i n g of Ag, Cd, Co, Cu, Pb and Zn among biding c o m p o n e n t s i m p o r t a n t in o x i d i z e d s e d i m e n t s , as i n d i c a t e d by s t a t i s t i c a l a s s o c i a t i o n s (from Luoma and Bryan, 1 9 8 1 ) . BIOAVAILABILITY PHYSICAL ENVIRONMENT ~1 Solution—J Specini Water - ^>l 1 ^ Form, 3. Upukf Partitioning —J Psnitionirm | ^ » ' ' ^ Sutairate^ A Suhstrzis. Environmental Ch»r»ct wit tics - «fUagoninic, tyn«rgitiic, »dditivt mteractiorn - lempwatura Figure 2 . A s i m p l i f i e d s h e m a t i c i l l u s t r a t i o n of t h e v a r i o u s p r o c e s s e s which a f f e c t t h e a v a i l a b i l i t y of t r a c e contaminants to organisms. 350 Figure 3. Differences in uptake of 1 1 0 m Ag when d i f f e r e n t type; of well-defined sediments were ingested by the depositf e e d i n g clam Macoma b a l t i c a . S e d i m e n t - t y p e s art amorphous i r o n o x i d e s (Fe), decaying marsh grass fragments (org), manganese oxides (Mn), crushed bivalve s h e l l s (BioCa), and c a l c i u m c a r b o n a t e (CaHfrom Luom< and Jenne, 1977). 351 s t a t i s t i c a l s t u d y , a s s e s s i n g c o r r e l a t i o n s of metal c o n c e n t r a t i o n s w i t h component c o n c e n t r a t i o n s among n e a r l y 50 g e o c h e m i c a l l y d i v e r s e s e d i m e n t s s t r o n g l y i n d i c a t e d the multi-component nature of m e t a l b i n d i n g ( F i g . 1; Luoma and B r y a n ) . More r e c e n t l y , a t t e m p t s t o c a l c u l a t e t h e o r e t i c a l metal d i s t r i b u t i o n s have shown t h a t a t l e a s t Cu i s m a i n l y d i s t r i b u t e d b e t w e e n i r o n o x i d e and o r g a n i c m a t e r i a l s in s e d i m e n t s , but t h e r e l a t i v e i m p o r t a n c e of e a c h d i f f e r s among s e d i m e n t s ( D a v i e s - C o l l e y 1 9 8 5 ; Luoma, in press). T h i s means t h a t no s i n g l e component d o m i n a t e s t h e p a r t i t i o n i n g of a m e t a l ; and t h a t p a r t i t i o n i n g may change from p l a c e to p l a c e or time t o t i m e . 2. BIOLOGICAL IMPACT OF VARIABLE METAL PARTITIONING. If m e t a l s p a r t i t i o n among a number of c o m p o n e n t s , t h e n organisms t h a t i n g e s t or c o n t a c t s e d i m e n t s are not exposed t o the sediment-bound metal as a s i n g l e e n t i t y . Rather, each metal i s encountered in a v a r i e t y of m e t a l - l i g a n d a s s o c i a t i o n s (Fig. 2); and t h a t v a r i e t y i s n o t c o n s t a n t in t i m e or s p a c e . Laboratory s t u d i e s c l e a r l y show t h a t each metal-component a s s o c i a t i o n has a d i s t i n c t l y d i f f e r e n t b i o l o g i c a l a v a i l a b i l i t y . Cadmium i s accumulated r a p i d l y by d e p o s i t f e e d i n g o r g a n i s m s - ( t h e clam Macoma b a l t h i c a ) from s e d i m e n t s c o n t a i n i n g o r g a n i c m a t e r i a l s such as the p o l y s a c c a r i d e e x o p o l y m e r s e c r e t e d e x t r a c e l l u l a r l y by some b a c t e r i a ( H a r v e y and Luoma, 1 9 8 5 ) . H o w e v e r , Cd i s n o t accumulated from s e d i m e n t s s t r i p p e d of o r g a n i c m a t e r i a l s or from p a r t i c u l a t e s t h a t are e i t h e r p u r e l y iron o x i d e s or are composed of iron o x i d e coated with l i v i n g b a c t e r i a (Luoma and Jenne 1976; Harvey and Luoma, 1985). The r a t e of uptake of Zn, Ag and Co may d i f f e r by o r d e r s of m a g n i t u d e when t h e s e m e t a l s a r e bound t o d i f f e r e n t s p e c i f i c c o m p o n e n t s . o f the sediment (Luoma and Jenne, 1977). For e x a m p l e , F i g . 3 s h o w s t h a t u p t a k e o f Ag by M. b a l t h i c a was 10 f o l d g r e a t e r when manganese o x i d e - b o u n d Ag was i n g e s t e d as compared t o i n g e s t i o n of Ag a s s o c i a t e d w i t h i r o n o x i d e s or o r g a n i c m a t e r i a l s (marsh g r a s s d e t r i t u s ) . T h u s , g e o c h e m i c a l s t u d i e s show t h a t t h e d i s t r i b u t i o n of a metal among components may vary from sediment t o s e d i m e n t , and l a b o r a t o r y b i o l o g i c a l s t u d i e s show t h a t a d i f f e r e n c e in component a s s o c i a t i o n of a m e t a l may c a u s e a d i f f e r e n c e i n m e t a l bioavailability. T h e r e f o r e , in n a t u r e m e t a l c o n c e n t r a t i o n s in o r g a n i s m s s h o u l d v a r y among s e d i m e n t s of d i f f e r i n g component concentrations. 3. COMPARISONS OF METALS IN ORGANISMS AND SEDIMENTS. In natural systems organisms are directly exposed to sediment-bound metals through surface contact, and accidental or intentional ingestion during feeding. Sediments also may control solute metal concentrations in waters in contact with the sediment bed sufficiently long to approach equilibrium, thus affecting biological exposures through the solute vector of uptake. Thus, metal tissue burdens in deposit and suspension feeding organisms should directly reflect the biological availability of sediment-bound metals. These organisms are exposed to all components of the sediment in their quest for nutrition. Most choose their food only on the basis of particle size, or particle density (Newell, 1965, Whitlach, 1974; Bubnova, 1974, Self and Jumars, 1978), although particle-size selectivity may differ among species. For example the clam, Macoma balthica, 352 d i g e s t s v a r i o u s t y p e s of p a r t i c l e s l e s s than 80 urn in s i z e (Yonge, 1949). The average p a r t i c l e s i z e in the d i g e s t i v e gland of Macoma i n q u i n a t a i s 10 urn, w h i l e p a r t i c l e s in t h e gut of îlâcoma s e c t a a v e r a g e 300 urn (Reid and R e i d , 1 9 6 9 ) . The more s e l e c t i v e f e e d e r , P e c t i n a r i a g o u l d i i (a p o l y c h a e t e worm), i n g e s t s p a r t i c l e s <75 urn, and >25 urn, but employs no d e t e c t a b l e chemical selection (Whitlach, 1974). Selective suspension-feeding o r g a n i s m s a l s o may i n a d v e r t e n t l y i n g e s t a v a r i e t y of m e t a l b i n d i n g s u b s t r a t e s when heavy c o n c e n t r a t i o n s of r e - s u s p e n d e d m a t e r i a l s a r e mixed w i t h p h y t o p l a n k t o n in t h e w a t e r c o l u m n , or may employ some s u s p e n d e d s e d i m e n t as an e s s e n t i a l s o u r c e of nutrition. Most b e n t h i c organisms a l s o are exposed p r i m a r i l y to m e t a l s a s s o c i a t e d w i t h o x i d i z e d p a r t i c l e s (Luoma and D a v i s , 1 9 8 3 ) . In oxgenated w a t e r s , reducing c o n d i t i o n s occur in sediments below t h e s e d i m e n t - w a t e r i n t e r f a c e , but a t h i n l a y e r of o x i d i z e d sediment i s l e f t at the sediment water i n t e r f a c e . Many i n f a u n a l o r g a n i s m s f e e d a t t h e o x i d i z e d s e d i m e n t - w a t e r i n t e r f a c e , or i r r i g a t e borrows with water from the o x i d i z e d s u r f a c e . Meiofauna l i v e e x c l u s i v e l y above t h e redox i n t e r f a c e ( C o u l l , 1 9 7 9 ) , and e p i b e n t h i c organisms are in c o n t a c t , almost e x c l u s i v e l y , with the o x i d i z e d e n v i r o n m e n t a t t h e s u r f a c e of t h e s e d i m e n t . Where reducing conditions occur, they undoubtedly a f f e c t the a v a i l a b i l i t y of s e d i m e n t - b o j i n d m e t a l s ; but i n g e n e r a l t h e o x i d i z e d s u r f a c e l a y e r of s e d i m e n t s i s much more i m p o r t a n t b i o l o g i c a l l y than i n d i c a t e d by i t s mass. If e x p o s u r e s t o s e d i m e n t s c o n t r o l b i o a c c u m u l a t i o n by benthos, then metal c o n c e n t r a t i o n s in organisms in nature might c o r r e l a t e with c o n c e n t r a t i o n s in s e d i m e n t s . Strong c o r r e l a t i o n s are most commonly not o b s e r v e d , h o w e v e r . . Poor c o r r e l a t i o n s b e t w e e n m a r i n e or e s t u a r i n e b e n t h i c o r g a n i s m s and t h e i r s e d i m e n t a r y h a b i t a t have been r e p o r t e d by C r o s s e t a l . , ( 1 9 7 0 ) , Halcrow, e t a l . , (1973), V a l i e l a e t a l . , (1974), Huggett e t a l . , ( 1 9 7 5 ) , Luoma ( 1 9 7 7 b ) , and S c h n e l l and N e v e s s i ( 1 9 7 7 ) . The poor c o r r e l a t i o n s between metal c o n c e n t r a t i o n s in b e n t h i c organisms and s e d i m e n t s c o u l d mean t h a t m e t a l in b e n t h o s are not d e r i v e d from s e d i m e n t s , or s o u r c e s coupled t o s e d i m e n t s . However, they could a l s o r e s u l t from s t a t i s t i c a l problems in the comparison or from t h e i n f l u e n c e of v a r i a b l e s o t h e r than s e d i m e n t a r y m e t a l c o n c e n t r a t i o n s upon metal b i o a v a i l a b i l i t y . Two e s p e c i a l l y i m p o r t a n t p r o b l e m s have c h a r a c t e r i z e d s t a t i s t i c a l comparisons of metal c o n c e n t r a t i o n s in benthos and t h e i r f o o d : (1) t h e a c t u a l food of t h e o r g a n i s m s has not a l w a y s been used in t h e c o m p a r i s o n ; and (2) an a d e q u a t e d a t a range has not always been employed. O b v i o u s l y , metal c o n c e n t r a t i o n s in f i l t e r - f e e d i n g organisms such as o y s t e r s , m u s s e l s and some s p e c i e s of c l a m s ( t h a t are d e p e n d e n t p r i m a r i l y upon phy t o p l a n x t o n f o r f o o d ) o r i n herbivorous g r a z i n g a n i m a l s , would not n e c e s s a r i l y c o r r e l a t e with metal c o n c e n t r a t i o n s in s e d i m e n t s , even i f food were the primary v e c t o r of m e t a l u p t a k e . For e x a m p l e , c o n c e n t r a t i o n s of most m e t a l s in g r a z i n g s n a i l s f o l l o w c o n c e n t r a t i o n s in a l g a e , but not s e d i m e n t s , where s e d i m e n t s and a l g a e a r e not c o r r e l a t e d (Bryan and Hummerstone, 1977; Young, 1975). Even among d e p o s i t - f e e d i n g 353 organisms, d i f f e r e n c e s in food sources may affect metal exposure. For e x a m p l e , P h e l p s (1967) and P h e l p s , e t a l . , (1969) r e p o r t e d c o n s i s t e n t d i f f e r e n c e s in Zn c o n c e n t r a t i o n s among b e n t h i c p o l y c h a e t e s from d i f f e r e n t f e e d i n g g u i l d s ( s u r f a c e f e e d e r s vs. subsurface f e e d e r s ; s e l e c t i v e vs. n o n - s e l e c t i v e feeders). Most c o r r e l a t i o n s t u d i e s also have been conducted within a s i n g l e body of w a t e r , i n c l u d i n g only narrow c o n c e n t r a t i o n g r a d i e n t s in the comparison. Comparisons which have considered wider d a t a r a n g e s have shown some s i g n i f i c a n t c o r r e l a t i o n s b e t w e e n m e t a l c o n c e n t r a t i o n s i n d e p o s i t f e e d e r s and c o n c e n t r a t i o n s in s e d i m e n t s . Bryan (1974) found that c o n c e n t r a t i o n s of Cu, Pb, and Cd in t h e p o l y c h a e t e N. d i v e r s i c o l o r c o r r e l a t e d s t r o n g l y with concnetrations in sediments from the sediment-water i n t e r f a c e when data were c o l l e c t e d from several estuaries. Packer e t aj. (1980) found t h a t Cd and Zn c o n c e n t r a t i o n s in the polychaete Arenicola marina followed Cd and Zn in s e d i m e n t s from 24 s t a t i o n s on t h e c o a s t of W a l e s . S i g n i f i c a n t c o r r e l a t i o n s were not observed for Pb, Cu, and Mn, however. In an e x t e n s i v e s u r v e y , Luoma and Bryan (1978, 1979, 1982) compared c o n c e n t r a t i o n s of Ag, Cd, Co, Cu, Pb and Zn in two deposit f e e d e r s , the burrowing clam S c r o b i c u l a r i a plana and the polychaete N^ d i v e r s i c o l o r , to concentrations in sediments over a wide range of conditions among 50 s t a t i o n s in 17 e s t u a r i e s . The d a t a range for a l l m e t a l s was two to t h r e e o r d e r s of m a g n i t u d e . S t a t i s t i c a l l y s i g n i f i c a n t (but weak) c o r r e l a t i o n s between t o t a l m e t a l s in s e d i m e n t s and t h e t i s s u e s of S. p l a n a were observed for Pb ( F i g . 4 ) , and for a l l o t h e r m e t a l s e x c e p t Cu. Stronger 10 1.000 100 I 1 10,0 1 I 1 Aooo E > r H i.ooo • > •• • ; \ SO J > -J • •• j | SOO • • • • XL* • • • • 1 30 i 1 1 _ 5O0 1 S,0OO CONCENTRATION OF Pb IN S E D I M E N T (jjg/g) Figure 4. Correlation of Pb in surficial estuarine sediments with Pb in the deposit-feeding bivalve Scrobicularia plana. r = 0.69 for power function fit. Data from 17 estuaries (from Luoma and Bryan, 1978). 354 Figure 5A) Concentrations of Cu observed in the soft tissues of M, balthica in South San Francisco Bay" between June 1975 and June 1983. Rep resentative errors bars (one SEM) areshown in 1979. B) Salinity observed at same station in water in the mantl e cavity of M. balti< C) Cu discharge from the sewage treatment works located 1 km south of above station. D) HCL-extractable Cu in surficial sediments ( <100um grain size) at same. station. !.. 1975 1 1 1977 . 1 -..I.. 1979 -I • 1. — 1981 I I 1983 .001 .01 1 1 0.10 ' 1.000 Figure 6. Correlation of Pb in 5. plana with ratio of P'o/fe (both extracted by IN HC1) in surficial esturarine sediments. r = 0.95. Data from 17 estuaries (from Luoma and Bryan, 1978). 300 - SO / •• • J t J PbHCI/FeHC! -- 1.0 1 355 correlations were observed between sediments and N^_ diversicolor for Cu and Pb. However, over the broader data set, these correlations were not as strong as observed by Bryan (1974.) In general, the data suggested that total concentrations contributed to metal concentrations in the deposit feeders, but that an understanding of other contributing variables would be necessary to predict metal concentrations in organisms from concentrations in the environment. Sediments need not be the only source of metal exposure for benthic organisms. Deviations in correlations between organisms and sediments could result from uptake from solution. However, even where the source of exposure which controls both the food and solute vectors is well-defined, deviations of bioaccumulation from dependence upon exposure alone are evident. For example, Bryan and Hummerstone (1977) observed differences in Ag and Cu concentrations in S. plana from two estuaries that could not be explained by Ag and Cu either in water or in sediment. In San Francisco Bay, spatial variations in Cu concentration indicated a sewage outfall was the primary source of the metal for the burrowing clam M^ balthica (Thomson et al., 1984). However comparisons of nine years of near-monthly analyses of plant effluent, and clams from this site showed that, although Cu levels in M^ ^âitîli^Ë were occas s ional ly coupled to Cu discharges, large fluctuations in concentrations occurred in the clam which could not be explained by changes in exposure (Fig. 5). Again, a general dependence upon exposure was evident, but other variables were also obviously important in controlling bioaccumulation. Recent studies strongly indicate that one of the most important of those factors is the chemical characteristics of the sediment. The importance of such characteristics was first clearly demonstrated by Luoma and Bryan (1978). As previously mentioned, concentrations of Pb in the deposit feeding bivalve Scrobicularia plana were significantly correlated with concentrations of Pb in sediments from 37 stations in 17 estuaries in southwest England (Fig. 4) in that study. However, the correlation was characterized by substantial variability. It was noticed that the stations with unusually high Pb concentrations were stations where the ratio between Pb and extractable Fe* was also high. Among all stations concentrations of Pb in S^_ Plana were very closely correlated (R2 = 0.89) with Pb/Fe in sediments (where Fe was measured by HC1 extraction, Fig. 6). Luoma and Bryan (1978) suggested that the availability of Pb was enhanced at low concentrations of Fe in sediment because less Pb was strongly bound to iron oxides as the Pb/Fe ratio in sediments increased making more Pb biologically available in the digestive tract. Whatever the cause, the ratio Pb/Fe, in sediments was an accurate predictor of Pb in S^ elâHâ * n estuaries not included in the original regression calculation *Fe extracted either with 1NHC1 for two hours or 0.4N acid ammonium oxalate for two hours—presumably an amorphous fraction of iron oxide. 356 HCl-soluble Pb ( u g / g ) Estuary Pb o b s e r v e d i n S^ p l a n a (ug/g) Pb p r e d i c t e d i n S. p l a n a from Pb/Fe in sediment Axe 25 8 9 Thames 57 25 36 Elorn 71 31 34 E. 93 104 128 Gannel 417 327 330 Humber 191 22 28 Looe Table 1. The c o n c e n t r a t i o n o f Pb o b s e r v e d i n s e d i m e n t s (HCl e x t r a c t i o n ) and s o f t t i s s u e s o f Scrob.icul.ar_ia p l a n a from s i x e s t u a r i e s compared w i t h t h e c o n c e n t r a t i o n of Pb p r e d i c t e d for S. planci from t h e Pb/Fe r a t i o in t h e s e d i m e n t s . Data from Luoma and Bryan ( 1 9 7 8 ) . Best Extraction Method Inhibits Enhances Vector Availability Availability Ag HCl sediment (interstitial water) Cu e x t r a c t a b l e Fe? As Total sediment solute (polychaetes) e x t r a c t a b l e Fe Cd HCl solute sediment anoxia (S=) Co HCl sediment (solute?) o r g a n i c carbon Cu Total HCl sediment (polychaetes) e x t r a c t a b l e Fe o r g a n i c carbon? anoxia sediment o r g a n i c carbon e x t r a c t a b l e Fe moderate Eh low o r g a n i c carbon Total HCl sediment e x t r a c t a b l e Fe o r g a n i c carbon 1N_ ammonium acetate HCl sediment o r g a n i c carbon Hg Pb Zn i Table 2. sewage f a c t o r sewage f a c t o r ? (molluscs) solute Summary of various factors which appear to i n h i b i t or enhance the a v a i l a b i l i t y of sediment-bound trace metals to benthic organisms. 357 (Table 1). In e s t u a r i e s s u c h a s t h e L o o e , Pb i n S_^ p l a n a was g r e a t e r t h a n in e s t u a r i e s such as L'Elorn in F r a n c e , a l t h o u g h Pb c o n c e n t r a t i o n s in s e d i m e n t were s i m i l a r , b e c a u s e e x t r a c t a b l e Fe was l o w e r in t h e Looe. The most d r a m a t i c example was t h e Humber, w h i c h i n c l u d e s t h e i n d u s t r i a l M i d l a n d s of E n g l a n d in i t s watershed. Although s e d i m e n t s were h i g h l y c o n t a m i n a t e d w i t h Pb, t h e s t a t i s t i c a l m o d e l p r e d i c t e d l i t t l e Pb s h o u l d o c c u r in S. p l a n a i n t h e Humber b e c a u s e of t h e v e r y h i g h Fe c o n c e n t r a t i o n s in the sediment. O b s e r v a t i o n s proved t h i s t o be t h e c a s e . S i m i l a r t o P b , L a n g s t o n ( 1 9 8 0 ; 1982) h a s shown t h a t l e v e l s of As i n S^ p l a n a and M_^ b a l t h i c a a r e a l s o b e s t r e l a t e d t o t h e A s : F e r a t i o in a IN HC1 e x t r a c t of s u r f a c e s e d i m e n t . M e r c u r y , on t h e o t h e r h a n d , h a s a h i g h a f f i n i t y f o r o r g a n i c p a r t i c l e s and c o n c e n t r a t i o n s in £^._ p l a n a and M_^ b a l t h i c a a r e r e l a t e d t o t h e t o t a l (HNO3 e x t r a c t a b l e ) H g : t o t a l o r g a n i c m a t t e r r a t i o s i n t h e <100 urn f r a c t i o n of s u r f a c e s e d i m e n t s ( L a n g s t o n , 1982). T h i s a g r e e s w i t h t h e work of B r e t e l e r e t a l . (1981) which showed t h a t t h e h i g h e s t c o n c e n t r a t i o n of Hg in m u s s e l s (Modiolus d e m i s s u s ) and c r a b s ( Uca p_u£n.aj£) o c c u r r e d i n a n i m a l s e x p o s e d t o s e d i m e n t s h a v i n g low l e v e l s of o r g a n i c m a t t e r . P h y s i o c h e m i c a l c o n d i t i o n s o t h e r than sediment component c o n c e n t r a t i o n s also appear to influence metal b i o a v a i l a b i l i t y from s e d i m e n t . F o r e x a m p l e , t h e a v a i l a b i l i t y of Ag ( w h i c h a p p e a r s in t h e s e d i m e n t s of t h e S e i n e in c o n c e n t r a t i o n s h i g h e r t h a n r e p o r t e d anywhere in t h e w o r l d ) t o d e p o s i t f e e d i n g b i v a l v e s i s s t r o n g l y r e d u c e d when h i g h c o n c e n t r a t i o n s of Cu a p p e a r i n s e d i m e n t s (Luoma and B r y a n , 1 9 8 2 ) . I n c r e a s e d pH a p p e a r s t o i n c r e a s e a v a i l a b i l i t y of Hg ( p e r h a p s by s t i m u l a t i n g c o n v e r s i o n of Hg t o Hg°), but n o t Cu and Pb t o marsh p l a n t s (Gambrell e t a l . , 1 9 7 7 ) . U n p u b l i s h e d d a t a from t h e s t u d y of Luoma and Bryan a l s o s u g g e s t e d Cd was of l o w e r a v a i l a b i l i t y in h i g h l y a n o x i c m u d f l a t s (e.g., inner Poole Harbor). The a v a i l a b i l i t y of Cu t o t h e p o l y c h a e t e Naanthes a r e n a e o d e n t a t a a l s o i s l e s s from s u b s u r f a c e t h a n from s u r f a c e s e d i m e n t s ( P e s c h , 1 9 7 9 ) , p r e s u m a b l y due t o d i f f e r e n c e s in redox p o t e n t i a l . In c o n t r a s t , c e r t a i n t y p e s of r e d u c i n g c o n d i t i o n s e n h a n c e d t h e b i o a v a i l a b i l i t y of Cu t o t h e an c l a m s £3^ P_iana ^ M^ b§_Ith_ica (Luc-ma a n d B r y a n , 1 9 8 2 ) . E x c e p t i o n a l l y h i g h c o n c e n t r a t i o n s of Cu w e r e o b s e r v e d i n t h e s e a n i m a l s in seven a n o x i c m u d f l a t s , and d u r i n g an u n u s u a l p e r i o d of a n o x i a on one m u d f l a t . G r e a t e r enhancements of Cu a v a i l a b i l i t y g e n e r a l l y accompanied lower c o n c e n t r a t i o n s of Fe in s e d i m e n t s , b u t t h e p r e c i s e c a u s e of t h e enhancement was not i d e n t i f i e d . In a r e c e n t r e v i e w , Bryan (1985) s u m m a r i z e d , for a number of t r a c e m e t a l s , t h e r e s u l t s of h i s e x t e n s i v e e x p e r i e n c e , and t h a t of o t h e r s , w i t h p r o c e s s e s c o n t r o l l i n g m e t a l a v a i l a b i l i t y from sediments to aquatic organisms. I t must be e m p h a s i z e d t h a t t h e s e conclusions are preliminary. R e s u l t s s o m e t i m e s d i f f e r e d among s p e c i e s , and d e f i n i t i v e s t u d i e s have o n l y been c o n d u c t e d w i t h a few s p e c i e s , m o s t l y i n e s t u a r i n e e n v i r o n m e n t s . From B r y a n ' s s u m m a r i z a t i o n and o u r e x p e r i e n c e , t h e f o l l o w i n g c o n c l u s i o n s a p p e a r : ( 1 ) High c o n c e n t r a t i o n s of o r g a n i c m a t t e r a n d / o r Fe ( p r o b a b l y a s a m o r p h o u s i r o n o x i d e ) i n h i b i t t h e a v a i l a b i l i t y of Hg, P b , A s , Zn, and p o s s i b l y Ag and Cu. S e d i m e n t s h i g h i n t o t a l o r g a n i c carbon or e x t r a c t a b l e Fe may c o n t a i n h i g h c o n c e n t r a t i o n s of t r a c e m e t a l s , but t h e m e t a l s do n o t a p p e a r t o p a s s on t o most biota. (2) Under some c i r c u m s t a n c e s o r f o r some s p e c i e s , t h e 358 s o l u t e v e c t o r o f u p t a k e i s an e s p e c i a l l y i m p o r t a n t s o u r c e o f Cd, Z n , a n d p o s s i b l y As a n d A g . (3) T o t a l c o n c e n t r a t i o n s in s e d i m e n t s c o n t r o l Cu a v a i l a b i l i t y to p o l y c h a e t e s , but the c o n t r o l s on Cu a v a i l a b i l i t y t o m o l l u s c s a r e n o t c l e a r . Anoxia m a y e n h a n c e Cu a v a i l a b i l i t y to mulluscs# under some circumstances. ( 4 ) Zn a v a i l a b i l i t y i s c o n t r o l l e d by r e a d i l y e x c h a n g e a b l e Zn i n s e d i m e n t , u p t a k e f r o m t h e s o l u t e v e c t o r , and a negative influence of o r g a n i c carbon. (5) Most metals ( e s p e c i a l l y Hg, P b , Zn, A s , Cu, and Ag) w o u l d be e x p e c t e d t o be of h i g h b i o a v a i l a b i l i t y i n c o a r s e r g r a i n e d s e d i m e n t s e n r i c h e d by a n t h r o p o g e n i c m e t a l i n p u t and i n w a s t e s ( s u c h a s s m e l t e r w a s t e s or mine w a s t e s ) l o w in o r g a n i c m a t e r i a l or Fe. Some u n k n o w n a t t r i b u t e o f s e w a g e s l u d g e e n h a n c e s t h e a v a i l a b i l i t y o f Ag a n d p o s s i b l y Cd. Table 2 summarizes the c o n c l u s i o n s p r e s e n t e d to d a t e on f a c t o r s c o n t r o l l i n g m e t a l a v a i l a b i l i t y from s e d i m e n t s t o benthos. 4.RECOMMENDATIONS TREATMENTS . FOR IMPROVING BIOLOGICAL RELEVANCE OF SEDIMENT I t m u s t be r e - e m p h a s i z e d t h a t o u r k n o w l e d g e o f metal b i o a v a i l a b i l i t y from s e d i m e n t s i s , at b e s t , fragmentary. D e f i n i t i v e s t u d i e s are l e s s than f i v e y e a r s o l d , have been c o n d u c t e d by o n l y a f e w r e s e a r c h g r o u p s , c o n s i d e r o n l y a f e w s p e c i e s , and n e a r l y a l l h a v e been c o n d u c t e d i n e s t u a r i e s . Nearly a l l c o n c l u s i o n s r e s t upon s t a t i s t i c a l e v i d e n c e w h i c h h a s n o t y e t been m e c h a n i s t i c a l l y c l a r i f i e d by d e f i n i t i v e l a b o r a t o r y s t u d i e s . A d d i t i o n a l c o m p a r a t i v e s t u d i e s among e s t u a r i e s , r i v e r s o r c o a s t a l e n v i r o n m e n t s a r e n e e d e d , a s a r e c o n t r o l l e d s t u d i e s , t e s t i n g some of t h e h y p o t h e s e s g e n e r a t e d by t h e s t a t i s t i c a l work. W i t h i n t h e l i m i t a t i o n s of our p r e s e n t k n o w l e d g e , i t is p o s s i b l e t o recommend a few p r a c t i c a l p r o c e d u r e s which c o u l d enhance t h e b i o l o g i c a l r e l e v a n c e of s e d i m e n t t r e a t m e n t . However, i t m u s t be a c c e p t e d t h a t t h e s e r e c o m m e n d a t i o n s a r e p r e l i m i n a r y and c o u l d c h a n g e a s o u r k n o w l e d g e g r o w s . Furthermore, the o b j e c t i v e i s t o recommend t h e s i m p l e s t p o s s i b l e p r o c e d u r e s , s o a s t o m a x i m i z e t h e i r u t i l i t y i n an o p e r a t i o n a l p r o g r a m . The s i m p l e s t , could include: b i o l o g i c a l l y r e l e v a n t measurements of sediments (1) Measurement of t o t a l c o n c e n t r a t i o n s (or n e a r - t o t a l using an HN0 3 -reflux) of t r a c e m e t a l s . (2) A s i m p l e e x t r a c t i o n of s e d i m e n t s w i t h a 0.5N HCl. and a n a l y s i s of t r a c e m e t a l s in the e x t r a c t . (3) Measurement of major s e d i m e n t c o m p o n e n t s which a f f e c t bioavailability. These i n c l u d e : (a) Total organic carbon. (b) Concentrations of Fe extracted by HCl. (Acid ammonium o x a j a t e is a m o r e w i d e l y a c c e p t e d a l t e r n a t i v e for estimating amorphous Fe oxide. However, HCl and oxalate extractions of estuarine sediments usually yield similar results. For the sake of smplicity, measurement of Fe in the same HCl extract used for metals would not result in much loss of information.) (c) Total Mn. 359 Collection of such samples should be from microenvironments of most relevance to organisms of interest in the systems involved. In estuaries such as the Seine, this usually means sediments should be collected carefully from the thin oxidized layer at the sediment-water interface. Sediments should be seived prior to storage. We employ a 100 urn seive, others suggest 60 urn. Sediments also should be frozen as soon as possible if they are to be stored prior to extractions, so as to prevent redox changes which could affect extraction results. This simple program would provide information about the major consitiuents that appear to affect metal bioavailability, and concentrations of metals that may competitively inhibit availability. From such a program, general assessments of the vulnerability of different sedimentary environments to accumulation of biologically significant concentrations of trace metals could begin to be possible. Breteler R. J., Valiela I & Teal J. M. (1981). - Bioavailability of mercury in several north-eastern U.S. Spa£t_ina ecosystems. Estuarine, Coastal Shelf Sci^ 12:155-166. Bryan G. W.(1974). - Adaptation of an estuarine sediments containing high concentrations of ^n: Pol-luti^qn and Physiology of Marine Vernber^ âQ<! !ÎLL Yernberg (eds.} t Academic 123-136. Bryan polychaete to heavy metals, OE^âHisnis^ ^_i Press, London, G. W., and Hummerstone L. G. (1977). - Indicators of metal contamination in the Looe estuary (Cornwall) particular regard to silver and lead, Jour. Mar^ Biol. U.K.. 57, 75-92. Bryan G. W. (1985). - The biological availability and effects of heavy metals in marine deposits. Wastes in the Sea Vol. 6, Near Shore Waste Disposal (in press). Bubnova N. P. (1974).- Consumption and assimilation of carbohydrates from marine sediments by the detritus-feedinq mollusks Macoma balthica (L.) and Portlandia arctica (Gray), Oceanography 14, 743-747. Coull Cross B. C.C1979). - Aspects of benthic-pelagic coupling in estuarine systems, Presented at Fifth Biennial International Estuarine Res. Conf., Jekyll Island, Georgia. F. A., Hardy L. H., Jones F. 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