Physiological responses of estuarine animals to cadmium pollution

Helgoland Marine Research, May 2019

Toxic effects of cadmium contamination may be observed at all levels of organismic organization. In estuarine areas the sensitivity of euryhaline species to acute Cd toxicity is strongly modified by various abiotic factors, whereas long-term threshold values are less dependent on environmental parameters. Experiments with larval stages of the molluscMytilus edulis reveal that Cd effects on life functions such as development and growth are differentially modified by temperature and salinity. High Cd concentrations can be accumulated by adult bivalves of coastal areas without signs of physiological damage. Mechanisms of heavy-metal detoxication in these molluscs seem to be quite different from those known to exist in vertebrates. Among decapod crustaceans, stenoecous species tend to exhibit higher rates of Cd uptake than euryoecous ones. Rates of Cd uptake and of accumulation depend on external and internal factors. In adultNereis succinea individuals sublethal Cd effects have been recorded on growth and food conversion (in terms of energy content).

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Physiological responses of estuarine animals to cadmium pollution

HELGOL~NDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. P h y s i o l o g i c a l r e s p o n s e s of e s t u a r i n e a n i m a l s to c a d m i u m p o l l u t i o n Toxic effects of cadmium contamination may be observed at all levels of organismic organization. In estuarine areas the sensitivity of euryhaline species to acute Cd toxicity is strongly modified by various abiotic factors, whereas long-term threshold values are less dependent on environmental parameters. Experiments with larval stages of the mollusc Mytilus edulis reveal that Cd effects on life functions such as development and growth are differentially modified by temperature and salinity. High Cd concentrations can be accumulated by adult bivaives of coastal areas without signs of physiological damage. Mechanisms of heavy-metal detoxication in these molluscs seem to be quite different from those known to exist in vertebrates. Among decapod crustaceans, stenoecous species tend to exhibit higher rates of Cd uptake than euryoecous ones. Rates of Cd uptake and of accumulation depend on external and internal factors. In adult Nereis succinea individuals sublethal Cd effects have been recorded on growth and food conversion (in terms of energy content). - H. T h e e d e GENERAL A S P E C T S OF TOXICITY The m e c h a n i s m of c a d m i u m toxicity is c o m p l e x and not yet fully understood. Indication of the toxic effects of i n c r e a s e d Cd l e v e l s m a y b e found at all IeveIs of o r g a n i s m i c structure and function. At t h e m o 1 e c u 1 a r 1 e v e 1 e s s e n t i a l m e t a l s at active sites of e n z y m e s or m e m b r a n e p r o t e i n s are c o m p e t i t i v e l y e x c h a n g e d b y Cd. Its r e a c t i o n w i t h b i o l o g i c a l l y active g r o u p s (e. g. carboxyl, p h e n o x y l , s u l p h h y d r i l , d i s u l p h i d e a n d p h o s p h a t e groups) s e e m s to b e of b a s i c s i g n i f i c a n c e for its toxic a c t i o n ( F r i b e r g et al., 1976) . M a n y e n z y m e s are k n o w n to b e i n h i b i t e d b y C d (e. g. ATPase, p h o s p h a t a s e , c a r b o h y d r a s e , p e p t i d a s e , a l d o l a s e ) (Vallee & Ulmer, 1972; S c h r 6 d e r & Alsen, 1976) . H o w e v e r , in specific c a s e s the vast n u m b e r of p o s s i b l e i n t e r a c t i o n s m a k e s it difficult to p i n p o i n t the m a i n m o l e c u l a r c a u s e s of toxic effects. At the s u b c e 11 u 1 a r 1 e v e 1, M o o r e & S t e b b i n g (1976) f o u n d in m a r i n e h y d r o i d p o l y p s that C d m a y w e a k e n the l y s o s o m e m e m b r a n e s a n d c a u s e s l y s o s e m a l e n z y m e s to b e r e l e a s e d to the cell. The c a u s e s for c e l l u l a r dysfunctions u n d e r the i n f l u e n c e of C d h a v e to b e s o u g h t in the a b o v e - m e n t i o n e d m o l e c u l a r a n d s u b c e l l u l a r effects. For e x a m p l e , d e c r e a s e d a b s o r p t i o n of calcium, iron (Larsson et al., 1976) a n d a m i n o a c i d s (Siebers & Ehlers, 1979) a n d t h e r e d u c t i o n of active r e a b s o r p t i o n b y k i d n e y t u b u l i cells m a y b e d u e to t h e i n h i b i t i o n of c e r t a i n active t r a n s p o r t m e c h a n i s m s . M e m b r a n e perm e a b i l i t i e s also s e e m to b e affected. In v e r t e b r a t e s (fish a n d m a m m a l s ) the k i d n e y a p p e a r s to b e the critical o r g a n (for l i t e r a t u r e consult: F r i b e r g et al., 1976; S c h r 6 d e r & Alsen, 1976; U m w e l t b u n d e s a m t , 1977) . W h e n a c e r t a i n C d l e v e l (about 200 #g g-1 fresh w e i g h t in the r e n a l cortex) is r e a c h e d , d y s f u n c t i o n of t u b u l i results in e x c r e t i o n of h i g h q u a n t i t i e s of proteins, a m i n o acids, glucose, c a l c i u m a n d p o t a s s i u m in the urine. This has g r e a t i n f l u e n c e on the c o m p o s i t i o n of the blood. Loss of Ca l e a d s to b o n e d e c a l c i f i c a t i o n , s k e l e t a l d e f o r m a t i o n , b o n e s h o r t e n i n g a n d b r i t t l e n e s s in " i t a i i t a i " d i s e a s e . In addition, l a c k of Ca a n d K has n e u r o m u s c u l a r effects. O t h e r o r g a n s - the l u n g s in t e r r e s t r i a l a n d gills in a q u a t i c a n i m a l s , the l i v e r a n d h o r m o n e systems (e. g. the a d r e n a l cortex s y s t e m a n d the i n s u l i n p r o d u c i n g B-cells in the p a n c r e a s ) - m a y also b e a f f e c t e d b y C d c o n t a m i n a t i o n (cf. Scholz et al., 1978). A t t h e o r g a n i s m i c l e v e l in v e r t e b r a t e s , " i t a i itai" d i s e a s e with k i d n e y d a m a g e , Ca loss a n d the a b o v e - m e n t i o n e d , p a i n f u l s k e l e t a l d e f o r m a t i o n s h a v e b e e n d e s c r i b e d b y F r i b e r g et al. (1976). In v e r t e b r a t e s a n d i n v e r t e b r a t e s , effects of C d on g r o w t h ( S t e b b i n g , 1976~ Paffenh6fer, 1978; y o n W e s t e r n h a g e n et al., 1978; S t e b b i n g & H i b y , 1979) , e m b r y o a n d l a r v a l d e v e l o p m e n t ( C a l a b r e s e et al., 1973; M i r k e s et al., 1978; Reish & C a r r , 1978; A l d e r d i c e et al., 1979; KI6ckner, 1979; L e h n b e r g & T h e e d e , 1979) , a n d the a l t e r a t i o n of v a r i o u s p h y s i o l o g i c a l functions (e. g. o s m o r e g u l a t i o n , excretion, respiration) (MacInnes & T h u r b e r g , 1973; T h u r b e r g et al., 1973; D a w s o n et al., 1977; T h u r b e r g et al., 1977) a n d b e h a v i o u r (Martin et al., 1975; E l d o n & Kristoffersson, 1978) h a v e b e e n o b s e r v e d . E F F E C T S OF E N V I R O N M E N T A L F A C T O R S O N TOXICITY W h e r e e c o l o g i c a l l y v a l i d c o n c l u s i o n s are sought, only s e n s i t i v e s p e c i e s are s u i t a b l e as t e s t o r g a n i s m s for the i n d i c a t i o n of toxic s u b s t a n c e s . T h e s e are, for e x a m p l e , l a r v a e of oysters a n d c r u s t a c e a n s or fish e m b r y o s , w h i c h are c o n s i d e r a b l y m o r e s e n s i t i v e to h e a v y m e t a l s t h a n a r e the r e p r o d u c t i v e a d u l t stages. M a r i n e h y d r o i d p o l y p s also r e s p o n d s e n s i t i v e l y to h e a v y m e t a l s (Karbe, 1972; S t e b b i n g , 1976; Fischer, 1978) : e. g. L a o m e d e a loveni r e s p o n d s e v e n to c a d m i u m c o n c e n t r a t i o n s in t h e low #g 1-1 r a n g e (Scholz et al., 1978; T h e e d e et al., 1979b) . H o w e v e r , e x p e r i m e n t a l d e t e r m i n a t i o n of t o l e r a n c e limits m u s t t a k e a b i o t i c e n v i r o n m e n t a l factors into account, b e c a u s e t h e y m a y b e of i m p o r t a n c e for in-situ survival, e s p e c i a l l y in e s t u a r i e s a n d coastal a r e a s (Eisler, 1971; O l s o n & Harrel, 1973; von W e s t e r n h a g e n et al., 1974; Jones, 1975; R o s e n b e r g & Costlow, 1976; Sullivan, 1977; V o y e r et al., 1977; W e i s & Weis, 1978; L e h n b e r g & T h e e d e , 1979; T h e e d e et al., 1979b) . W e h a v e s t u d i e d the effects of t e m p e r a t u r e a n d s a l i n i t y on the a c u t e toxicity of c a d m i u m in m a r i n e H y d r o z o a . It was c l e a r l y s h o w n that the s u s c e p t i b i l i t y to c a d m i u m of the h y d r o i d p o l y p L a o m e d e a l o v e n i d e p e n d s s i g n i f i c a n t l y on t e m p e r a t u r e a n d s a l i n i t y (Fig. 1). The p o l y p s are most t o l e r a n t to C d at low t e m p e r a t u r e s a n d h i g h salinities. At h i g h e r t e m p e r a t u r e s a n d l o w e r s a l i n i t i e s t h e y are m o r e sensitive. After 7 d a y s of e x p o s u r e at 17.5 ~ a n d 10 %0 S, i r r e v e r s i b l e r e t r a c t i o n of 50% of the h y d r a n t h s t a k e s p l a c e at a c o n c e n t r a t i o n of --3 fig C d 1-L This c o n c e n t r a t i o n is only a b o u t 5 - 6 t i m e s h i g h e r t h a n the h i g h e s t C d c o n c e n t r a t i o n r e c o r d e d in t h e h e a v i l y c o n t a m i n a t e d i n n e r Kiel F j o r d (western Baltic Sea). It is 10-100 t i m e s h i g h e r t h a n the e s t i m a t e d a v e r a g e C d c o n c e n t r a t i o n in the Baltic S e a ( T h e e d e et al., 1979b) . T h e s e results i n d i c a t e that m a r i n e o r g a n i s m s l i v i n g n e a r t h e i r d i s t r i b u t i o n a l limits u n d e r e s t u a r i n e or the b r a c k i s h - w a t e r c o n d i t i o n s of the Baltic S e a t e n d to suffer from c o n s i d e r a b l y l o w e r p o l l u t i o n l e v e l s t h a n those l i v i n g u n d e r o p t i m a l e n v i r o n m e n t a l conditions. C o n s e q u e n t l y , critical limits for a c u t e toxicity e s t a b l i s h e d u n d e r n o r m a l m a r i n e c o n d i t i o n s m a y not a u t o m a t i c a l l y b e a p p l i c a b l e to c o n d i t i o n s p r e v a i l i n g in e s t u a r i e s or in the Baltic S e a ( T h e e d e et al., 1979b) . This m a y also e x p l a i n the m o r e 1o / =- / I ~, eo I .I Fig. 2. Clava multicornis. Changes of the modifying effects of temperature and salinity during transition from acute to chronic toxicity of cadmium. The graph indicates the upper limits of Cd concentrations at which feeding responses occurred (after Fischer, 1978; and Scholz et al., 1978) ASPECTS O F A C C U M U L A T I O N A N D E L I M I N A T I O N In contrast to the a b o v e - m e n t i o n e d c n i d a r i a n s a n d l a r v a l stages, a d u l t m o l l u s c s (Brooks & Rumsby, 1967; Eisler et al., 1972; N i c k l e s s et al., 1972; P e d e n et al., 1973; Phillips, 1976a) a n d a d u l t c r u s t a c e a n s (Wright, 1977a, b, c) are a b I e to a c c u m u l a t e h i g h a m o u n t s of h e a v y m e t a l s w i t h o u t o b v i o u s n e g a t i v e effects. W e c o m p a r e d m u s s e l s from different l o c a l i t i e s of the G e r m a n coasts ( T h e e d e et al., 1979a) . In m a n y p l a c e s of the w e s t e r n Baltic S e a the l e v e l s of C d in Mytilus edulis are h i g h e r t h a n in c o m p a r a b l e i n d i v i d u a l s from l o c a l i t i e s of the North Sea coast. The C d c o n c e n t r a t i o n s are e s p e c i a l l y h i g h in m u s s e l s from Kiel h a r b o u r , w h e r e t h e r e is s e v e r e w a t e r c o n t a m i n a t i o n d u e to local i n d u s t r i e s a n d h a r b o u r facilities as w e l l as the t o w n ' s r a i n w a t e r d r a i n a g e system. Thus C d contents of m u s s e l s from the i n n e r p a r t of the Kiel F j o r d r a n g e up to 30 m g k g -1 (per dry w e i g h t of soft parts). In the o u t e r p a r t of the Kiel Bay C d v a l u e s in m u s s e I s g e n e r a l l y r a n g e b e t w e e n 1 a n d 4 m g k g -1. T h e h i g h c a p a c i t y of m u s s e l s for a c c u m u l a t i n g h e a v y m e t a l s is one r e a s o n for c o n s i d e r i n g t h e s e a n i m a l s as s u i t a b l e o r g a n i s m s f o r m o n i t o r i n g h e a v y - m e t a l p o l l u t i o n (Phillips, 1976a; b) . S c h u l z - B a l d e s (1973) a n d Scholz (1980) f o u n d a p a r t i a l l i n e a r r e l a t i o n b e t w e e n h e a v y - m e t a l content of sea w a t e r a n d t h a t of mussels. H o w e v e r , t h e s e a n i m a l s a b s o r b h e a v y m e t a l s not o n l y from t h e w a t e r a n d t h e i r o r g a n i c food b u t also from i n o r g a n i c p a r t i c u l a t e matter. Bottom d w e l l e r s m a y t a k e in m o r e Cd, e. g. b y filtration of s u s p e n d e d o r g a n i c a n d i n o r g a n i c m a t t e r c o n t a i n i n g Cd. T h e r e f o r e m u s s e l s from the sea floor often t e n d to h a v e a h i g h e r C d content t h a n s p e c i m e n s l i v i n g further a b o v e the b o t t o m (e. g. on piles). T h e r e are also correlations of C d content in m u s s e l s w i t h size of the i n d i v i d u a l s a n d s e a s o n ( T h e e d e et al., 1979a) . It m u s t also b e c o n s i d e r e d that u p t a k e rates m a y s t r o n g l y d e p e n d on a b i o t i c factors l i k e t e m p e r a t u r e a n d osmotic v a l u e of the s e a w a t e r (Phillips, 1976; G e o r g e et al., 1978) . In a d d i t i o n , e l i m i n a t i o n rates in m a r i n e i n v e r t e b r a t e s m a y b e r e l a t i v e l y h i g h u n d e r c e r t a i n conditions. Vertebrates, w h i c h are a b l e to store fairly large q u a n t i t i e s of h e a v y metals i n liver a n d k i d n e y b y b i n d i n g t h e m to special metalloproteins, so-called m e t a l l o t h i o n e i n s , h a v e l o n g b i o l o g i c a l half times for Cd i n the m a g n i t u d e of m o n t h s or years (Table 1). However, i n invertebrates, e. g. Carcinus m a e n a s a n d M y t i l u s eduHs, biological half times bet w e e n 11/2 w e e k s a n d a b o u t two m o n t h s were observed w h e n the a n i m a l s h a d a c c u m u lated h i g h a m o u n t s of c a d m i u m from the water u n d e r e x p e r i m e n t a l conditions. However, according to P e d e n et al. (1973) there was almost no e l i m i n a t i o n of this m e t a l w i t h i n 3 to 7 weeks, w h e n Carcinus m a e n a s , Patella vulgata a n d N u c e l l a lapillus i n d i v i d u a l s , w h i c h h a d a c c u m u l a t e d c a d m i u m u n d e r c o n t a m i n a t e d field conditions (Cd content of sea w a t e r 0.01 m g 1-1) w e r e transferred to a n u n c o n t a m i n a t e d estuary (0.0002 m g Cd 1-1). The r a n g e s of the half times f o u n d i n d i c a t e that the m e t a l m a y b e b o u n d w i t h i n different c o m p a r t m e n t s (Coombs & George, 1979; J a n s s e n & Scholz, 1979; Scholz, 1980) , from w h i c h it will be r e l e a s e d at different rates. In addition, the difference i n half times of v e r t e b r a t e s a n d i n v e r t e b r a t e s raises the q u e s t i o n w h e t h e r there are f u n d a m e n t a l differences in the m e c h a n i s m of h e a v y - m e t a l detoxication i n both systematic groups. This point is dealt with in detail b y Scholz (1979, 1980). I should like to add a few remarks on some recently observed i n f l u e n c e s of s u b l e t h a l Cd c o n t a m i n a t i o n on m e t a b o l i c processes of adult invertebrates. In d e c a p o d crustaceans it has b e e n observed that Cd u p t a k e rate decreases in the order: E u p a g u r u s bernhardus > Carcinus m a e n a s > Hriocheir sinensis. In this s e q u e n c e the last species is the most e u r y h a l i n e a n d euryoecous one. W h e n these a n i m a l s are fed w i t h M y t i l u s food a n d k e p t for 4 w e e k s i n sea w a t e r with different Cd concentrations, there is a n i n c r e a s e i n w a t e r content i n the c o n t a m i n a t e d animals: At a b o u t 100 #g Cd 1-1 the w a t e r content of B u p a g u r u s i n c r e a s e d by n e a r l y 10 %; at a b o u t 500 #g Cd 1-1 the effect i n Hriocheir s i n e n s i s is a n increase of about 2.5 % ( u n p u b l i s h e d results of T h e e d e & Baukloh). In M e t r i d i u m s e n i l e the p r o t e i n content decreases more n o t i c e a b l y w h e n the a n i m a l s are fed or starved i n C d - c o n t a i n i n g water. The effect is more p r o n o u n c e d i n the smaller i n d i v i d u a l s , which take u p Cd more rapidly. In a n i m a l s o b t a i n e d from their n a t u r a l h a b i t a t a n i n v e r s e r e l a t i o n b e t w e e n Cd c o n t e n t a n d p r o t e i n c o n t e n t a p p e a r s to exist (Theede & Baukloh, u n p u b l i s h e d ) . 0.50 "0 Alderdice, D. P., Rosenthal, H. &Velsen, F. P. J., 1979. Influence of salinity and cadmium on capsule strength in Pacific herring eggs. - Helgol~inder wiss. Meeresunters. 32, 149-162. Brooks, R. R. & Rumsby, M. G., 1967. Studies on the uptake of cadmium by the oyster Ostrea sinuata {Lamarck). - Aust. J. mar. Freshwat. Res. 18, 53-61. Calabrese , A. , Collier , R. S. , Nelson , D. A. & MacInnes , J. R. , 1973 . The toxicity of heavy metals to embryos of the A m e r i c a n oyster Crassostrea virginica . - Mar. Biol . 18 , 162 - 166 . Calabrese , A. , Thurberg , F. P. & Gould , E. , 1977 . Effects of cadmium, mercury and silver on marine animals . - Mar. Fish. Rev . 39 ( 4 ), 5 - 11 . Coombs , T. L. & George , S. G. , 1978 . M e c h a n i s m s of immobilization and detoxication of metals in marine organisms . In: Physiology and behaviour of marine organisms . Ed. by D. S. McLusky & A. J. Berry. P e r g a m o n Pl;ess , Oxford, 179 - 187 . Dawson , M. A. , Gould , E. , Thurberg , F. P. & Calabrese , A. , 1977 . Physiological r e s p o n s e of juvenile striped bass, h/Iorone saxatilis, to low levels of c a d m i u m and mercury. - C h e s a p e a k e Sci . 18 , 353 -- 359 . Douglas-Wilson , L , 1972 . C a d m i u m pollution a n d itai itai disease . - Lancet I , 382 - 383 . Eisler , R. , 1971 . C a d m i u m poisoning in F u n d u l u s heteroclitus (Pisces: Cyprinodontidae) and other marine organisms . - J. Fish. Res. Bd Can . 28 , 1225 - 1234 . Eisler , R. , Zaroogian , G. E. & Hennekey , R.J. , 1972 . C a d m i u m uptake by marine organisms . - J. Fish. Res. Bd Can . 29 , 1367 - 1369 . Eldon , J. & Kristoffersson , R. , 1978 . 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H. Theede. Physiological responses of estuarine animals to cadmium pollution, Helgoland Marine Research, 26, DOI: 10.1007/BF02414732