HELGOLANDER MEERESUNTERSUCHUNGEN Helgol~inder Meeresunters. 33, 6-25 (1980)

Recent trends in r e s e a r c h o n h e a v y - m e t a l

c o n t a m i n a t i o n in the sea

G. W. Bryan

Marine Biological Association of the United Kingdom, the Laboratory, Citadel Hill; Plymouth PL1 2PB, U. K.

ABSTRACT: Recent trends in the study of metal contamination in the sea are reviewed. Aspects of contamination which are considered include the input of metals to the sea and their deposition in the sediments, the influence of environmental and biological factors on the accumulation of metals by the biota and the use of organisms as indicators of contamination. Laboratory studies on the biological effects of metals and the problem of monitoring effects in the field are discussed. The importance of the metabohsm of metals by the biota is stressed since it is relevant to the adaptation of organisms to chronic contamination and to the attainment of very high levels in some commercial species. Finally, the abatement of contamination is discussed.

INTRODUCTION

St imulated by factors such as the mercury problem and the deve lopment of rapid analyt ical t echniques there has over the past 10 years b e e n a spectacular increase in research on heavy-meta l contamina t ion in the sea. Heavy metals are of course na tura l const i tuents of the mar ine envi ronment , a lbei t sometimes at very low levels, and 11 at least (Fe, Cu, Zn, Co, Mn, Cr, Mo, V, Se, Ni, Sn) appear to be biological ly essential . As metal loproteins or meta l -pro te in complexes they occur in enzymes and respiratory pigments , for example, and may have a structural role in polychaete jaws (cf. O'Del l & Campbel l , 1971; Bryan & Gibbs, 1979). As a result, studies on metal con tamina t ion encounter the problem of d i s t inguish ing be t w e e n na tura l levels and those which are e n h a n c e d from anthropogenic sources and may, since metals are demonst rably toxic, produce undes i r ab le effects.

Al though from a publ ic heal th aspect, Hg, Cd and Pb are considered the most hazardous metals and the first two occur on various b lack lists, several others inc lud ing Cu, Zn, Ag and Cr may be of equal or greater hazard to mar ine biota.

The object of this paper is to review briefly recent ideas about various aspects of the problem of heavy-meta l con tamina t ion in the sea.

THE FATE OF HEAVY METALS IN THE SEA

Metals from anthropogenic sources reach the sea via rivers and outfalls, a tmospheric fallout, dumping , mar ine m i n i n g and dril l ing, and from ships. With the increas ing avai labi l i ty of information it has become possible to compare the magn i tude of na tura l

�9 Biologische Anstalt Helgoland 0017-9957/80/0033/0006/$ 02.00

Heavy-metal contamination in the sea 7

and anthropogenic inputs; for example, Goldberg et al. (1977) concluded that anthropogenic inputs to Narraganset t Bay exceeded natural levels by factors of 79 for Cu, 56 for Pb and 21 for Zn. In some areas the relative importance of different routes of input has been assessed; thus Cambray et al. (1979) showed that the atmospheric inputs of most heavy metals to the North Sea equal led in magni tude those from the River Rhine. Release of metals to the atmosphere raises the possibili ty of global contamination and a recent assessment (Nriagu, 1979) suggests that global emissions of Cd (smelting) and Pb (petrol) exceed natural inputs by well over an order of magnitude. There is evidence suggest ing that whereas contamination from other sources tends to be local, atmospheric inputs may have enhanced surface sea-water concentrations of metals including Hg and Pb on a regional scale (cf. Windom et al., 1975).

E s t u a r i n e d e p o s i t i o n of m e t a l s

Since some of the most heavi ly industr ial ised areas of the world are sited on the banks of estuaries, these waters are part icularly at risk from metall ic contamination. In the past, metall ic wastes have been discharged into rivers and estuaries based on the assumption that they would be carried to the open sea and dispersed. The truth of the matter is somewhat different and Turekian (1977) has emphasised the efficiency of estuaries as traps where heavy metals are deposited.

Two of the most important components in the deposition process are Fe and the humic materials which stabilize it and other colloidal constituents in river water (cf. Sholkovitz, 1978). The increase in salinity and sometimes pH during estuarine mixing leads to the flocculation of iron oxides, the associated humic substances and other materials such as clays, which are then deposi ted together with their adsorbed trace metals (cf. Davies & Leckie, 1978). Deposition is often assisted by biological processes such as the production of faeces or pseudofaeces by filter feeders; indeed, in the oceans, the residence times of many metals are primarily controlled by faecal deposition (Cherry et al., 1978).

Examples in Figure 1 show the "soluble" concentrations of Fe, Cu, Zn and Mn change during estuarine mixing in Restronguet Creek, a branch of the Fal estuary system, which receives acid metalliferous mining wastes via the River Carnon. The initial fall in concentrations is the result of dilution with uncontaminated water from another river, but the cross-hatched areas below the theoretical lines for simple mixing of sea water and river water show the degree of flocculation of the different metals; whereas Fe is almost completely removed from "solution" and Cu largely so, Mn and Zn exhibit far less tendency to be removed. A comparison between concentrations in the inflowing river (largely in solution, pH 3.9) and the Creek sediments is shown in Table 1, and the degree of retention of metals by the sediments, assuming that Fe is 100 % retained, is also shown and compared with values from other areas. The high degree of retention of Pb and As may relate to their adsorption by oxides of Fe or, as is more l ikely for Cu, by the associated humic materials. Possibly by virtue of their high concentrations in the river Mn and Zn show little retention, as also does Cd which forms strong chloride complexes in sea water and is not readi ly removed from solution (cf. Sholkovitz, 1978).

Although the behaviour of Fe in Figure 1 is commonly found, t he degree of removal (cross-hatched areas) of other metals varies considerably between estuaries (cf. Beau-

G. W. Bryan

5 I 0.5

0 10 20 30 Satinity

2.4 ~ 3.9

o

2.2 , 1 2.0 ~ 1.8 1.6 ~,

e 1.z, ""'i &t2

1.0

0.8

0.6

0.4

0.2

i

0

)H8.O

o ~

: i I; ' 2b 3'o So~Linity

36 Ca

Fig. 1. Restronguet Creek: relations between salinity of water and "soluble" concentrations of four metals. Shaded areas below lines for simple dilution indicate degree of removal of metal from

"solution'r

l ieu: Ho l l iday & Liss, 1976; Rhine: Du inker & Nol t ing, 1978). Indeed, in some es tuar ies such as the Tamar, concentra t ions of Mn, Zn and Cu have b e e n obse rved to p e a k at i n t e rmed ia t e sal ini t ies , sugges t ing remobi l i za t ion from the sed iments or desorp t ion from s u s p e n d e d par t ic les (Bryan & Hummers tone , 1973; Morr is et al., 1978). Redox condi t ions are pa r t i cu la r ly r e l evan t to the r emobi l i za t ion of meta l s from sediments ; r educ ing condi t ions t end to promote the so lub i l iza t ion of Mn and Fe, w he re a s ox id i s ing condi t ions a p p e a r conducive not only to the r e l ease of Cd, Cu, Ni, Pb and Zn (Lu & Chen, 1977) bu t also to the mic rob io log ica l me thy la t ion of Hg which is suspec ted to be the o r ig ina l source of me thy l mercury in mar ine o rgan isms {cf. Pagers t r6m & Jernel6v, 1973~ Bart let t et al., 1978). The remobi l i za t ion of meta ls in es tuar ine sed imen t is no gua ran t ee that they wil l r each the sea since, as Tu rek i an (1977) has po in t ed out, r e l e a s e d meta l s are qui te l ike ly to be car r ied ups t r eam by the es tuar ine c i rcula t ion and redepos i t ed . The depos i - t ion of very h igh concentra t ions of h e a v y meta l s in the sed imen t s of many es tuar ies (and other conf ined areas) p rovides a s ink for con t inued con tamina t ion even in the absence of fur ther input and demons t ra tes c lear ly the unsu i t ab i l i ty of es tuar ies for heavy meta l disposal .

A v a i l a b i l i t y of m e t a l s for b i o a c c u m u l a t i o n

It is not p roposed to discuss the mechan i sms of me ta l absorp t ion by the b io ta (cf. Bryan, 1979) bu t ra ther to cons ider the in f luence on u p t a k e of different meta l l i c forms. Some of the ea r l i es t s tudies on this aspec t were conce rned wi th the formula t ion of more

Heavy-meta l contamina t ion in the sea 9

Table 1. Relation between metal concentrations in Carnon River and Restronguet Creek sediment

As Cd Cu Fe Mn Pb Zn

160

1080"

81

Total concentration in River Carnon (ppb) 22 615 7310 957 40 7585

Total concentration in Restronguet Creek sediment (ppm) 3" 3190 60900 403 379 2400

Percentage retention of river input by sediment assuming Fe -- 100 % 1.6 62 100 5 114 3.8

Percentage retention by southeastern USA estuaries (Windom, 1976) 17 - 100 64 - -

Percentage retention in Chesapeake Bay (Helz, 1976) 22 20 89 26 23 26

* Thornton et al. (1975)

deadly ant i foul ing paints. For example, it was shown that the greater toxicity of alkyl than inorganic Hg compounds to crustaceans probably results because their greater l ipid solubil i ty facilitates rapid pene t ra t ion of the ep idermal cell walls (cf, Corner & Rigler, 1958). Recent work has confirmed these observations on Hg in various phyla (cf. Pentreath, 1976a; Fowler et al., 1978) and studies have b e e n ex tended to inorganic and organic species of other metals. Since the culture media often conta in chelators, a n u m b e r of studies have b e e n concerned with the inf luence of na tura l and synthetic complexing agents on metal accumula t ion by phytoplankton: for example Sunda & Gui l lard (1976) showed that in such media the avai labi l i ty of Cu is reduced, the concentrat ions in the ceils be ing related to the cupric ion activity of the water and not the total Cu concentrat ion. On the other hand, the uptake of Cu by the polychaete Cirrifor- mia spirabrancha was unaffected by dissolved yeliow organic matter (Milanovich et al., 1976) and in Mytilus edulis George & Coombs (1977) observed that complexat ion of Cd with EDTA, alginic acid, humic acid or pect in actual ly doubled the rate of uptake and the final concentra t ion achieved. Others have b e e n concerned with the inf luence on uptake of inorganic forms of metals; for example, Fowler & Benayoun (1976) showed that Se was absorbed more readi ly as seleni te than selenate by M. galloprovincialis and studies on the up take of Cu, Cd, Pb and Zn in M. eduBs by Phill ips (1976) showed that only Cu uptake was in f luenced by the presence of the other metals.

Al though metals in solut ion are often in biological ly readi ly avai lable forms, the much h igher concentrat ions in other phases such as part iculates and food organisms often renders them far more important as sources of metals in mar ine animals. It is hardly surpris ing that the dietary matrix should inf luence absorpt ion and Pentreath (1976b), for example, found that 80-93 % of methyl Hg was re ta ined from a diet of Nereis by the plaice Pleuronectes platessa but only 4-42 % from Mytilus. Similarly, Luoma & Jenne (1977) showed that the avai labi l i ty of s ed imen t -bound metals to the deposi t - feeding bivalve Macoma balthica was very dependen t on the composit ion of particles to which the metals were adsorbed.

Al though we know that the b ioaccumula t ion of metals and p resumably their toxic i ty is governed by their form, the recogni t ion and measu remen t of various species in the field has proved very difficult. In sea water work on metal speciat ion is only now moving

10 G. W. B r y a n

Table 2. Some propert ies of biological indicators of heavy-meta l contaminat ion

Species Feeding Substrate type

Estuarine tolerance Spooner & Moore {1940} Upst ream limit in Tamar Estuary (km from mouth}

Use as indicator 4- Appears to act as indicator 4, +Par t icular ly good accumulator ? Doubt about use R Definite regulatory ability ( ) Months for t ransplanted organisms

to equi l ibr ia te wi th new environ- ment

Ag Cd Cu Cr Hg

A s c o p h y l l u m - - rock 11 4- 4. 4. n o d o s u m (New growth relates to new

tissue may never F u c u s - - rock 21 4- 4- + 4- 4- ves i cu losus M y t i l u s filter rock 15 ?6 4- !11 4- + edu l i s

(>5m?) ( -3m)

Ostrea filter sed iment / 10 + + + edu l i s stones (>5m) (>5m?} Ceras toderma filter sediment 13 + + + e d u l e Scrobicular ia deposit sediment 18 4- + ? + + p lana (8m} (>12m) (8m) M a c o m a deposit sediment 15 4- 4- ? 4- 4- bal th ica N e r e i s deposit / sediment 23 + + + + + dlvers ico lor omnivore (life span of Littorina herbivore rock/ i 1 + + + + R ? l i t torea sediment Littorina herbivore rock/weed/ I1 + + + + + obtusata sediment Patel la herbivore rock 8 + + + + vulgata

(3m?) (>3m) N u c e l l a carnivore rock 5 4- 4- 4- 4- 4- lap i l lus (>4m) (>4m)

References: 1. Haug et al. (1974); 2. Melhuus et al. (1978); 3. Myklestad et al. (1978}; 4. Bryan & Hummers tone (1973}; 5. Morris & Bale (1975}; 6. Bryan & Hummers tone (1977}; 7. Seeliger & Edwards (1977); 8. unpubl i shed; 9. Boyden (1975}; 10. Boyden {1977); 11. Phillips (1977}; 12. Davies & Pirie (1978}; 13. Young et al. (1979}; 14. Simpson (1979); 15. Majori et al. (1978};

f r o m t h e f i e l d of t h e o r y i n t o t h a t of r e a l i t y w i t h t h e a i d of a n o d i c s t r i p p i n g v o l t a m m e t r y

a n d s p e c i f i c i o n e l e c t r o d e s , for e x a m p l e . In t h e c a s e of s e d i m e n t s , r e c o g n i t i o n of v a r i o u s

fo rms d e p e n d s m a i n l y o n c h e m i c a l e x t r a c t i o n p r o c e d u r e s l a r g e l y i n h e r i t e d f rom soi l

c h e m i s t s . T h e s e m e t h o d s a r e c e r t a i n l y u s e f u l b u t a r e r a r e l y if e v e r s p e c i f i c for a

p a r t i c u l a r f o r m a n d d e s c r i p t i o n s of s e d i m e n t f r a c t i o n s as " a d s o r b e d m e t a l s " or " o r g a n i -

c a l l y b o u n d " a r e o p e r a t i o n a l r a t h e r t h a n t r u e d e s c r i p t i o n s of t h e ex t rac t s .

B e c a u s e t h e s p e c i a t i o n of m e t a l s i n t h e e n v i r o n m e n t is l a r g e l y u n k n o w n i t is

H e a v y - m e t a l c o n t a m i n a t i o n in t he s ea 11

Influence of increasing size

Concentration rises (+) falls ( - ) remains constant (0)

Ni Pb Zn Ref. Ag Cd Cu Cr Hg Ni Pb Zn Ref.

+ + 1,2 environment but old 3 equilibriate)

+ + + 2,4,5 6,7,8

+ + + 9,10, 0 12,13

(>4m) (>5m) 10,12 14,15

+ + 9,10 0 {<5m) 10

+ + 78 + 6,9

@ 1 2 - - - - - - 1 0

0 - - 0 10

- 0 - - 16

+ + + + + 6 + / - (>12m) (>12m) (>12m)17

+ + + + 6 0

+ + / - + + + + + 6,7,18

+ 0 O + 0 + 8

+ + R 6,19 N 1 year)

+ + + R 6,21, 22

+ + + R 6,23

variable but not usually marked

0 0 - 10

+ + 6,22, + 24

(>3m) 20 + + 6,22 (3m) 20

- 1 0

- 8

16. Boyden (1974); 17. Bryan & Hummerstone (1978); 18. Bryan & Uysal (1978); 19. Bryan (1974); 20. Stenner & Nickless (1974); 21. Bryan {1979); 22. Nickless et al. (1972); 23. Young (1975); 24. Preston et al. (1972)

f r e q u e n t l y d i f f icul t to r e l a t e l a b o r a t o r y o b s e r v a t i o n s on m e t a l u p t a k e (or toxici ty) to t he

f i e ld s i tua t ion . As a resul t , f i e ld s tud ie s on the u p t a k e arid loss of m e t a l s h a v e r e c e n t l y

b e e n c o n d u c t e d by t r ans fe r r i ng a n i m a l s b e t w e e n c o n t a m i n a t e d a n d u n c o n t a m i n a t e d

a r ea s (Table 2). W h i l e th is t y p e of e x p e r i m e n t suffers f rom l a c k of control , t he l o n g p e r i o d s of ten r e q u i r e d for e q u i l i b r a t i o n w i t h t h e n e w e n v i r o n m e n t c e r t a i n l y e m p h a s i s e

t he d i f f icu l ty of d r a w i n g c o n c l u s i o n s f rom sho r t - t e rm l abo ra to ry e x p e r i m e n t s . F i e l d

s tud ies h a v e a lso b e e n u s e d to i den t i fy factors con t ro l l i ng the a v a i l a b i l i t y of meta l s .

12 G . W . Bryan

Luoma & Bryan (1978, 1979) c o m p a r e d the concentra t ions of var ious meta l s in the depos i t - f eed ing b iva lve Scrobicularia plana with the concentra t ions in chemica l extracts of surface sediments . The s tudy covered a la rge n u m b e r of es tuar ies so that the an imals came from sed imen t s which va r i ed w i d e l y in total me ta l concentra t ions and in the a b u n d a n c e of m e t a l - b i n d i n g subs t ra tes such as i ron and m a n g a n e s e oxides and organic matter . In the case of Pb, the concent ra t ion in the an ima l was a lmost d i rec t ly propor t ion- al to the Pb/Pe rat io in 1N HC1 or 25 % acet ic ac id extracts of surface sediment , i nd ica t ing that the b ind ing of Pb by oxides of Fe is an impor tan t control on its ava i l ab i l i ty to the animal .

B i o l o g i c a l f a c to r s in b i o a c c u m u l a t i o n

Al though meta l spec ia t ion has a g rea t inf luence on the b ioaccumula t ion of heavy metals , the me tabo l i sm of the me ta l in the o rgan ism has an impor tan t inf luence on the concentra t ions u l t ima te ly achieved; both factors are of course in f luenced by environ- men ta l pa rame te r s such as salinity, t empe ra tu r e and so on. If an o rgan i sm absorbs meta l s at a ra te p ropor t iona l to the env i ronmen ta l concent ra t ion there are at leas t th ree poss ib le types of re la t ion b e t w e e n the concentra t ions ach i eved by the t issues and those of the envi ronment . (1) The o rgan i sm excre tes the meta l at a rate p ropor t iona l to the body b u r d e n and therefore the concent ra t ion in the body is p ropor t iona l to env i ronmen ta l ava i l ab i l i ty and usua l ly r ema ins fair ly constant or tends to fal l wi th inc reas ing age (e .g . Mytilus edulis, Table 2). (2) The o rgan i sm has l imi t ed powers of excre t ion and tends to store a b s o r b e d metals . In this case the concent ra t ion in the o rgan ism m a y sti l l be d i rec t ly p ropor t iona l to env i ronmen ta l ava i l ab i l i ty but, unless it grows fast enough to d i lu te the metal , the l eve l in the body tends to increase wi th age (e. g. Scrobicularia plana, Table 2). (3) The o rgan i sm is ab le to inc rease the eff iciency of excre t ion in response to i nc reased absorp t ion and therefore the concent ra t ion in the body does not inc rease in propor t ion to env i ronmenta l ava i l ab i l i t y (cf. Tab le 2 for examples of these r egu la t i ng organisms). Gene ra l ly speak ing , the more h igh ly evo lved forms inc lud ing fish and d e c a p o d crus taceans t end to be the bes t regu la tors and the essen t ia l meta l s such as Zn and Cu are be t te r r e g u l a t e d than the non-essen t i a l such as Cd and espec ia l ly Hg.

F o o d c h a i n s a n d b i o m a g n i f i c a t i o n

In the context of the pa s sage of meta l s a long food chains, it is of some impor tance whe the r or not a p reda to r r egu la t e s meta l s and w he the r its d ie t consists of o rgan isms which do or do not regula te . For example , f lounder , Platichthys flesus, from the Severn Estuary hav ing a die t of Macoma balthica (non-regulator) con ta ined h ighe r levels of Zn than those hav ing a d ie t of c rus taceans and smal l fish which tend to r egu la t e Zn (Hardis ty et al., 1974). Some years ago it was tac i t ly a s sumed by many peop le that al l con taminan ts are b io log ica l ly magn i f i ed in the i r pa s sa ge a long food chains. It is not difficult to f ind e x a m p l e s where an imals conta in h ighe r me ta l concentra t ions than thei r d ie t (cf. Cd in two non-regula tors , Littorina obtusata and Fucus vesiculosus in Table 5). However , if one looks at the concentra t ions of meta l s over the whole spec t rum of organisms from phy top l ank ton to fish and mar ine mammals , the only me ta l for which there is ev idence of gene ra l b ioampl i f i ca t ion is mercury or, more specif ical ly , me thy l

Heavy-meta l con tamina t ion in the sea 13

mercury which does not appear to be regula ted by any of the lower organisms and the majori ty of fish, It was sugges ted (Bryan, 1979) that the deve lopment of demethy la t ion processes in a few predatory fish species and mar ine mammals is an evolut ionary response to biomagnif icat ion.

INDICATORS OF METALLIC CONTAMINATION

Al though sea-water analysis certainly has a place in the detect ion of meta l l ic contaminat ion, it has unt i l recent ly proved difficult to obta in mean ingfu l results in

oceanic areas because of addi t ional con tamina t ion dur ing sampl ing (cf. Bruland et al., 1979}. In addit ion, the var iabi l i ty of levels, par t icular ly in stratified t idal estuaries makes it difficult to obta in an in tegra ted picture without considerable sampl ing effort. By comparison, analyses of sediments are easy and have provided va luab le information not only about recent metal l ic inputs bu t also, from dated cores, about the history of con tamina t ion (cf. Goldberg et al., 1977).

However, analyses of water and sediments are rarely carried out with regard to biological avai labi l i ty and therefore, since this parameter is one of the prerequisi tes for pollution, there is a strong a rgument for the analysis of biological indicators. Such indicators should preferably be good accumulators of metals, of reasonable size and should reflect changes in env i ronmenta l availabil i ty; thus organisms hav ing an abil i ty to regula te metals are unsui tab le . Other desirable properties are that the organism should be widely distr ibuted, common, accessible, easily recognised, relat ively stationary, avai lable at all t imes of year and, for es tuar ine purposes, sufficiently tolerant of low salini t ies and high suspended solids to penet ra te a reasonable distance ups t ream (cf. Phillips, 1977}. The propert ies of some inter t idal ben th ic organisms which have proved useful as indicators in the Uni ted Kingdom are summar i sed in Table 2 and an indica t ion of the relat ive merits of some of these species as accumula to r s is g iven in Table 3. Because different species have different distr ibutions r ang ing from rocky shores to muddy estuaries and absorb metals from different sources, there is no universa l indicator

Table 3. Comparison of metal accumulation in indicator species from a site 2 km up East Looe Estuary contaminated with Ag and Pb. Highest concentrations are underlined

Species Mean dry weight ppm dry tissue soft parts

(g) Ag Cd Cr Cu Hg* * Ni Pb Zn

ffucus vesicu]osus Mytilus edulJs 0.24 Cerastoderma edule 0.28 Scrobicularia plana O. 15 NIacoma balthica 0.04 Nereis diversicolor 0.02 Littorina littorea 0.18 Patella vulgata 0.53 Nucella lapillus * 0.20

�9 0 �9 6 kin; * * Langston (unpublished)

0.7 1.1 1.9 12 0.09 11.3 17 190 0.2 2.3 2.5 9 0.39 2.6 45 113 2.4 0.7 1.9 10 0.26 54 5.3 54

56.4 1.2 3._33 300 0.47 14.5 189 1120 81.9 0.2 3.3 338 - 6.9 61 1010 4.2 0.4 0.3 60 0.11 3.5 25 258

30.0 1.6 0.5 154 0.37 2.8 17 232 5.6 5.6 0.5 18 0.26 2.3 30 145 4.2 16 5.6 141 0.92 4.1 7.1 520

14 G. W. Bryan

'% L/%o.

SILVER ppm dry

�9 < 1

�9 1-10 @ 10-100

@>I00 max

Bristol Channel " ' - ' ~ ' ~

BRISTOL

~.~wou~ ' '~

L l O O k m u

Fig. 2. South-west Britain: geographical distribution of Ag in whole soft parts of Scrobicularia plana. Open circles are equivalent levels i n Macoma balthica, the concentration ranges above being divided by 0.59. Results are for individual sites in Severn (la-4a, lb-10b} but in estuaries

1-26 and 5 a - l l a are mean values along estuary. Estuary 7 is Restronguet Creek

organism. Any reasonable moni tor ing programme should therefore involve analyses of several species (e. g. seaweed, filter feeder, deposit feeder) to try and assess contamina- t ion in different forms. Table 3 i l lustrates how contamina t ion with part iculate Ag was readi ly avai lable to the deposi t - feeding bivalves Scrobicularia plana and Macoma balthica but not to Mytilus edulis and Fucus vesiculosus two commonly used indicators. Because of inf luences such as those of size (Table 2) and condi t ion on metal levels in organisms, their use calls for uniformity of sampling. With Scrobicularia it was found

necessary to analyse animals of 4-cm shell length collected from mid-t ide level in ei ther spr ing or a u t u m n to avoid the b reed ing season (cf. Fig. 2). Partly because it has b e e n the subject of so much study Mytilus appears to have more than its share of problems as an indicator, part icularly with regard to ob ta in ing organisms of comparable size, condi t ion and so on at different sites. However, some of these problems have b e e n c i rcumvented with the use of caged, cul t ivated mussels of k now n age as indicators of Hg contamina- t ion (Davies & Pirie, 1978).

H e a v y - m e t a l con tamina t ion in the sea 15

Gene ra l l y speak ing , the bes t b io log ica l indica tors of me ta l l i c con tamina t ion are not the most commerc ia l ly v a l u a b l e species . Fish are g e n e r a l l y mon i to red from the pub l i c hea l t h aspect , but for most me ta l s a re poor indica tors of env i ronmen ta l contaminat ion . However , they a p p e a r unab l e to r egu la t e H g ( largely in the me thy l form) and are a r g u a b l y the bes t indica tors of env i ronmen ta l con tamina t ion wi th this metal , if size is t a k e n into account (cf. Phil l ips, 1977). A l inear re la t ion b e t w e e n H g levels in sea w a t e r and those in the musc le of var ious te leos ts has b e e n demons t r a t ed b y G a r d n e r (1978); concent ra t ion factors (wet basis) r a n g e d from 2.9 • 103 in the leas t con tamina ted to 10.6 x 103 in the most con t amina t ed inshore waters , poss ib ly ref lec t ing the t e n d e n c y for concent ra t ion-s ize regress ions for fish to s t eepen in con tamina t ed a reas (cf. Renzoni , 1976).

EFFECTS OF HEAVY METALS

E x p e r i m e n t a l s t u d i e s

There is no doubt that the LCs0 (median le tha l concentrat ion) app roach to heavy- me ta l toxici ty has p rov ided a wea l th of informat ion about the effects of different me ta l s on different spec ies and has r e v e a l e d the many factors, b io logica l , chemica l anal env i ronmen ta l which modify toxicity. Even after long exposure , LC50 concentra t ions ra re ly fal l in the r anges obse rved in the most con t amina t ed w a t e r s . Exper iments wi th some larva l o rgan i sms prov ide except ions and Ca lab re se et al. (1977) found an 8-10 day LC50 of 16 ppb of Cu (SW usua l ly < 1 ppb) for l a rvae of the b iva lve Mercenar ia

mercenar ia . Al though this app roach has r e l evance to smal l organisms, wh ich m a y accumula t e meta l s rap id ly , it has b e e n shown to be pa t en t ly unsa t i s fac tory for l a rge r organisms. Here, absorp t ion of the me ta l (and hence an effect ive dose) is often so s low that somet imes only r id icu lous ly h igh concentra t ions are effective in toxic i ty t e s t s hav ing dea th as the end point . An e x a m p l e in Tab le 4 for Ctenodr i lus serratus shows that a l though the 96 hour LCs0 for Cr was 4.33 p p m c o m p a r e d wi th 0.09 for Hg, the concent ra t ions which in t ime affected reproduc t ion were equa l at 0.05 ppm. The much lower toxici ty of Cr in the LCs0 test p r o b a b l y reflects its s lower u p t a k e by the worm and hence the s lower a t t a inmen t of an effective dose. Rate of up t ake is cer ta in ly one of the impor tan t factors on which the re la t ive toxici ty o f different meta l s depends : Tab le 4 shows how the toxici t ies of meta l s to N e r e i s d ivers icolor are c losely r e l a t ed to up t ake rates m e a s u r e d wi th rad ionuc l ides . A l though the dose to an o rgan i sm is ve ry impor tan t it is often difficult to define. It is not s imply the total l eve l in the body s ince this wi l l i nc lude meta l s in i m m o b i l i s e d forms. The rate of i n t ake is impor tan t be c a use this de t e rmines whe the r the o rgan i sm ' s de toxi f ica t ion m e c h a n i s m can cope or not: one of the ma in adap ta t ions found in me ta l - to l e ran t s t rains of var ious spec ies is a lower p e r m e a b i l - ity, a l though very h igh concent ra t ions of i m m o b i l i s e d meta l s m a y be found.

Some of the factors which inf luence toxici ty (e. g. form of meta l , in f luence of o ther chemicals , sa l in i ty and t empera tu re ) m a y be effective b e c a u s e they change the rate of absorp t ion or excret ion. However , less than op t imum l iv ing condi t ions (e. g. low food supply , low oxygen level , low sal ini ty) which stress the o rgan i sm are also impor tan t and are add i t ive to the effect of the meta l .

In the search for effects at rea l i s t ic concentrat ions , i nc reas ing number s of s tudies

16 G. W. Bryan

Table 4. Toxicity of metals to two polychaete species

Element Ctenodrilus serratus (Reish, 1978) 96 hour LC50 Significant suppres-

(ppm) sion of reproduction (ppm)

Nereis diversicolor (50 % SW) 192 hour LC50 Rate of absorption

(ppm) from 0.1 ppm (ppm dry wgt/day)

Hg 0.09 0.05 >0.1 52 Cu 0.3 0.1 0.27 16 Ag - - 0.5 9 Cr (6) 4.3 0.05 10 5 (approx.*) Zn 7.1 0.5 30 1.4 Cd >20 2.5 100 0.4

* Rate estimated by extrapolation from net uptake rate at higher concentrations

have cons ide red the sub le tha l effects of meta l s and have p rogress ive ly inc reased in sophis t icat ion. They inc lude m u l t i p a r a m e t e r phys io logica l , b iochemica l and histo- pa tho log ica l s tudies on exposed fish (cf. Ca lab re se et al., 1975), s tudies on the most vu lne rab l e s tages in life cycles such as the eggs and ear ly la rva l s tages of fish (cf. Blaxter, 1977), factor ia l expe r imen t s demons t ra t ing the c o m b i n e d effects of metal , sa l in i ty and t empe ra tu r e on la rva l d e v e l o p m e n t of shr imp (cf. McKenney & Neff, 1979), expe r imen t s wi th l abora to ry cul tures (e. g. po lychae tes , Reish, 1978) and of course the cont ro l led ecosys tem or p l a s t i c -bag expe r imen t s (cf. Steele, 1979). Even this sub- le tha l work has f requent ly fa i led to demons t ra te effects at rea l i s t ic me ta l concentrat ions . Taylor (1977a, b) summar i s ed informat ion on the sub- l e tha l effects of Hg and Cd and found that the lowest levels p roduc ing an effect were 0. i ppb Hg (SW -- 0.02 ppb) and 1 ppb Cd (SW -- 0. i ppb) but that 90 % of the resul ts were in the ranges > 5 ppb Hg and 50 p p b Cd. Some of the effects obse rved at rea l i s t ic leve ls wi l l be cons ide red briefly.

Ca lab re se et al. (1975) s tud ied the effects of exposure for 60 days to 5 ppb of Cd on the f lounder Pseudopleuronectes americanus. O x y g e n consumpt ion was dep re s sed in exc i sed gi l l t i ssue but no effects were obse rved on var ious haema to log i ca l pa rame te r s such as p l a s m a pro te in leve l and p l a s m a osmolal i ty . In addi t ion , no h i s topa tho log ica l effects were observed, but Gould (1977) showed that synthes is of Zn me ta l l oenzymes was s t imula ted so that a l though unde r a t tack from Cd thei r functions could cont inue at a nea r -no rma l rate. Adap t a t i on to exposure was also obse rved by Dawson et al. (1977) who showed that a l though the oxygen consumpt ion of exc i sed gi l l t i ssue from the s t r iped bass Morone saxatilis was dep re s sed after 30 days exposure to 0.5 ppb of Cd it had re tu rned to normal after 90 days. However , as Gould (1977) has po in t ed out, adap t ive processes involv ing enzymic changes wi l l be a d ra in on metabo l i c energy.

The poss ib i l i ty of effects of meta ls on fecundi ty and reproduc t ion is of par t i cu la r env i ronmen ta l impor tance and some species have b e e n found to be very sensi t ive. Por example , Mora i tou-Apos to lopou lou & Verr iopoulos (1979) showed that e g g produc t ion in the copepod Acartia clausi was inh ib i t ed by only I ppb of Cu (SW < 1 ppb) , and in the copepod Pseudodiaptomus coronatus Paffenh6fer & Knowles (1978) found that 5 ppb of Cd r e d u c e d the rate of reproduc t ion by 50 0/0 bu t had no effect on growth, food convers ion and so on. There is a cons ide rab le l i te ra ture on the effects of low levels of meta l s on the growth of phy top l ank ton popula t ions in cul ture (Davies, 1978), a l though it is often

H e a v y - m e t a l con tamina t ion in the sea 17

difficult to ex t rapo la te the resul ts to the field. However , s tudies on na tura l popu la t ions of phy top l ank ton have shown them to be qui te sensi t ive and Davis & Sleep (1979) showed that the carbon f ixat ion ra te was d e p r e s s e d by 15 p p b of Zn (SW ~ 1 ppb), a l eve l often e x c e e d e d in con tamina t ed areas.

The most ambi t ious e x p e r i m e n t a l s tudies on the effects of meta l s have b e e n the cont ro l led ecosys tem exper imen t s car r ied out in enclosures in the Saan ich Inlet. Results from these and expe r imen t s at Loch Ewe have b e e n r e v i e w e d by S tee le (1979). A l though some effects were appa ren t fo l lowing add i t ions of 1 p p b of Hg or 10 ppb of Cu to the enclosures , it p roved difficult in some cases to s epa ra t e the effects of the meta l s from the a d d e d s t resses of enclosure . In fact, S tee le poin ts out that la rge t ank expe r imen t s con ta in ing a s imple phy top lank ton , Tellina, pla ice food chain were more sens i t ive to meta l s than the more na tu ra l ecosystems, effects b e i n g obse rved on phy top l a nk ton at 3 p p b of Cu and on p la ice at 0.1 ppb of Hg.

It can be conc luded that in some species effects have b e e n obse rved expe r imen ta l l y at concent ra t ions coming wi th in the r ange of va lues for some con tamina ted estuar ies , fjords and coasta l regions . However , the concent ra t ions in such areas are not gene ra l l y so h igh that effects in the f ie ld are l ike ly to be i m m e d i a t e l y obvious.

E f fec t s of m e t a l s i n t w o c o n t a m i n a t e d e s t u a r i e s

There are r e m a r k a b l y few examples in the l i te ra ture concern ing de le te r ious effects on the mar ine env i ronment which can unequ ivoc a b ly be a t t r ibu ted to me ta l con tamina- t ion (e.g. M i n a m a t a Bay, Japan) . Obvious ly the p laces where effects should be sought are those where r e s idue ana lyses have shown there to be h igh levels of contaminat ion . Two Uni ted Kingdom es tuar ies coming into this ca tegory are cons ide red below.

Restronguet Creek

Rest ronguet C r e e k (Pig. 2) is a b ranch of the Pal Estuary sys tem and is heav i ly con tamina t ed wi th meta l s (Pig. 1, Table 1). The C r e e k is about 4 km long, a lmost dr ies out at low t ide and has b e e n con tamina ted for over 200 years. Examples of Cu and Zn concentra t ions in organisms a p p r o a c h i n g the i r ups t r eam l imits of d is t r ibut ion are g iven in Tab le 5 and rat ios showing thei r e n h a n c e m e n t above normal va lues are also given. E n h a n c e m e n t for Cu var ies from about two orders of m a g n i t u d e in s e a w e e d and po lychae te worms to low levels in the crab and f lounder where r egu la t ion p r o b a b l y occurs. Regu la t ion p r o b a b l y exp la ins the va r i ab i l i ty in Zn e n h a n c e m e n t both d i rec t ly and b e c a u s e some preda tors may feed on organ isms which a l r e a dy regula te . A l though copper is one of the most toxic meta l s and the inf luence of Zn and other meta l s in Table 5 migh t be expec t ed to be addi t ive , the va r ie ty of spec ies found in the Creek c lear ly resul ts from the i r g rea t ab i l i ty to hand l e h igh concent ra t ions of Cu and Zn. For example , this is inhe ren t in oysters w h e r e the immobi l i za t ion of Cu (and Zn) in a g ranu la r form in the amoebocy te s l eaves the an imals g reen in colour and ined ib l e but o therwise unaf fec ted (cf. Geo rge et al., 1978). Other spec ies a p p e a r to have a d a p t e d by exposure to metals . Carcinus maenas from the u p p e r C r e e k were pa r t i cu la r ly to lerant to Zn, most of the l a rge r C r e e k an ima l s in one expe r imen t b e i n g unaf fec ted by 10 p p m over a pe r iod of 38 days whereas 50 % of the normal crabs d i ed wi th in 6 days. The more to lerant an imals were gene ra l l y less p e r m e a b l e to zinc and pe rhaps be t te r e q u i p p e d to excre te it;

18 G . W . Bryan

however , the induc t ion of Zn me ta l lo th ione in may also be involved, hav ing b e e n obse rved in other spec ies of crabs by Olafson et al. (1979). In the po lychae te N e r e i s

d ivers icolor to le rance to bo th Cu and Zn appea r s to be gene t i ca l ly b a s e d (Bryan, 1976). To le rance to Cu obse rved in Fucus ves icu losus from this es tuary might also have a gene t ic bas is s ince this has b e e n obse rved in other s e a w e e d s (Russell & Morris, 1970). A l though hav ing a lower in i t ia l g rowth rate F. ves icu losus from the C r e e k was ab le to cont inue g rowing in wa te r con ta in ing 0.1 p p m of Cu which p r e v e n t e d growth in w e e d from other es tuar ies (Fig. 3). Ana lyses of the w e e d at the b e g i n n i n g and end of the expe r imen t s sugges t that the to lerant w e e d is p robab ly less p e r m e a b l e to Cu and that this coup led wi th growth d i lu t ion he lps to l imi t the concentrat ion.

6O

o~

~0

20

i-01ppmco-i i i , ', J ~ . ~ / e [ ;,o 7

o _ o Z/i -o- OonO

�9 , y ' / ! , cuppmd,y

.u,~ i i ~

- , i , ! , , 10 20 30 40

Days

Fig. 3. Fucus vesiculosus. Effect of Cu on growth and concentrations in plants from three contrasting estuaries. Each line represents three plants of about 3-crn initial length (17.5 S%o, 13 ~ continuous

light, no added nutrients)

Since there a p p e a r to be no non-meta l l i c con taminants of any s igni f icance in the Creek any effects on the d is t r ibut ion of the b io ta should be a t t r ibu tab le to heavy metals . The effects are cer ta in ly not as c lear-cut as might be expec ted , the most obvious b e i n g the absence of Scrobicularia p lana from la rge areas of the in te r t ida l muds where , unde r normal condi t ions, it wou ld account for an app rec i ab l e fraction of the total b iomass .

Severn Es tuary - Bristol C h a n n e l

As a resul t of indus t r ia l p rocesses such as smel t ing, the waters of the Severn Estuary (Fig. 2) are a p p r e c i a b l y con tamina ted wi th Cd (1.4-9.4 ppb) and other meta l s (Abdul lah & Royle, 1974). De tec tab le Cd con tamina t ion ex tends for some 200 k m and Table 5 i l lus t ra tes the e n h a n c e m e n t of both Cd and A g levels in spec ies co l lec ted towards the i r ups t r eam l imits of dis t r ibut ion. E n h a n c e m e n t of Cd in al l spec ies is consis tent ly high, a p p e a r i n g to ref lect qui te c losely the e n h a n c e m e n t in the wa te r (say 5 p p b d iv ide d by 0.1 ppb -- 50) and the inab i l i t y of most spec ies to r egu la t e Cd levels . The appa ren t indi f ference of these o rgan i sms to such h igh Cd levels res ides in most cases in the

Tab

le 5

, H

igh

met

al c

on

cen

trat

ion

s (d

ry b

asis

) in

bio

ta f

rom

tw

o c

on

tam

inat

ed

estu

arie

s

Res

tro

ng

uet

C

reek

S

ite

Sp

ecie

s C

op

per

(k

m f

rom

mo

uth

) p

pm

R

estr

. C

reek

p

pm

"n

orm

al"

Zin

c N

ote

s o

n m

etal

to

lera

nce

an

d i

mm

ob

iliz

atio

n

Res

tr.

Cre

ek

"no

rmal

"

2 F

uc

us

ve

sic

ulo

sus

1612

16

0 2

04

0

20

2 N

ere

is d

ive

rsic

olo

r 11

70

58

290

2

2 N

ep

hty

s h

om

be

rgi

21

16

11

8 48

3 2

2 S

cro

bic

ula

ria

pla

na

15

0 4

2580

7

0 O

stre

a e

du

lis

3870

45

14

900

9 --

1

Ch

lam

ys

vari

a

54

4 2

07

0

4

0.5

L

itto

rin

a o

btu

sata

13

00

13

828

7 2

Ca

rcin

us

ma

en

as

191

2-3

14

9 2

4 P

lati

ch

thy

s fl

esu

s 11

8 2

203

1 (l

iver

)

To

lera

nce

to

Cu

(F

ig.

3) m

ech

anis

m

un

kn

ow

n

Cu

an

d Z

n t

ole

ran

ce b

ased

o

n l

ow

er p

erm

eab

ilit

y

and

C

u s

tora

ge

1 P

oss

ibly

sam

e as

Ne

reis

bu

t le

ss g

oo

d 1

S

lig

ht

tole

ran

ce t

o C

u 1

. M

ay a

vo

id w

ors

t b

y s

hel

l cl

osu

re

Sto

rag

e of

Cu

an

d Z

n i

n a

mo

ebo

cyte

s 2

Sto

rag

e of

Zn

in

kid

ney

g

ran

ule

s (Z

n =

7.6

%

of d

ry k

idn

ey)

Cu

po

ssib

ly h

and

led

b

y h

aem

ocy

anin

sy

stem

Z

n t

ole

ran

ce b

ased

par

tly

on

lo

wer

per

mea

bil

ity

an

d

po

ssib

ly m

etal

loth

ion

ein

M

ay a

vo

id w

ors

t co

nd

itio

ns

and

ten

ds

to r

egu

late

b

oth

met

als

Sev

ern

E

stu

ary

C

adm

ium

S

ilv

er

pp

m

Sev

ern

p

pm

S

ever

n

"no

rmal

..

..

n

orm

al"

Sh

arp

nes

s P

uc

us

ve

sic

ulo

sus

58

58

6.6

33

Sh

arp

nes

s N

ere

is d

ive

rsic

olo

r 10

50

24

60

S

har

pn

ess

Ma

co

ma

b

alt

hic

a

9.4

47

100

100

Fo

nty

gar

y B

. M

yti

lus

ed

uli

s 3

60

60

- -

Po

rtis

hea

d

Pa

tell

a v

ulg

ata

28

9 29

12

7

Sh

eper

din

e L

itto

rin

a o

btu

sata

19

9 40

9

3 F

lath

olm

N

uc

efl

a l

ap

illu

s 3

725

72

- -

Cle

ved

on

C

arc

inu

s m

ae

na

s s

~1

00

10

0 -

- O

ldb

ury

P

lati

ch

thy

s fl

esu

s 8

~5

-

- -

Un

kn

ow

n

ho

w m

etal

s h

and

led

A

g m

ay b

e h

and

led

li

ke

Cu

1

Un

kn

ow

n

ho

w m

etal

s h

and

led

C

d m

etal

loth

ion

ein

in

du

ced

4

Cd

met

allo

thio

nei

n i

nd

uce

d 6

C

d m

etal

loth

ion

ein

po

ssib

ly i

nv

olv

ed

Cd

met

allo

thio

nei

n

ind

uce

d

Cd

met

allo

thio

nei

n

ind

uce

d 7

C

d m

etal

loth

ion

ein

po

ssib

ly i

nv

olv

ed

o o i.-~

~

Ref

eren

ces:

1.

Bry

an (

1976

); 2

. G

eorg

e et

al.

(19

78);

3.

Nic

kle

ss e

t al

. (1

972)

; 4.

No

61

-Lam

bo

t (1

976)

; 5.

Ped

en e

t al

. (1

973)

; 6.

Ho

war

d

& N

ick

- le

ss (

1977

); 7

. Je

nn

ing

s et

al.

(19

79);

8.

Har

dis

ty e

t al

. (1

974)

20 G . W . Bryan

induct ion of me ta l lo th ione ins (Table 5). E n h a n c e m e n t of A g was par t i cu la r ly obvious in the bu r rowing spec ies but how it is h a n d l e d in Macoma balthica is unknown.

A s tudy of faunis t ic records cover ing the last 30 years (Mettam, 1979) ind ica tes that the total n u m b e r of spec ies in the es tuary has r e m a i n e d re la t ive ly constant and there is no ev idence for l ong- t e rm env i ronmen ta l changes . As wi th Res t ronguet Creek, however , con tamina t ion in the a rea is long s t and ing (cf. Clif ton & Hamil ton, 1979) and there is no cer ta in base l ine wi th which to compare .

M o n i t o r i n g t h e e f f ec t s of h e a v y m e t a l s

Al though de le te r ious effects m a y be obse rved in the field, the complex i ty of con tamina t ion in many a reas m a k e s it difficult to unequ ivoca l ly re la te effects to specif ic pol lutants . Since it demons t ra tes exposure , and also p r e s u m a b l y the u t i l iza t ion of ene rgy by the o rgan i sm to detoxify metals , r e s idue analys is is an obvious p re l imina ry to any a t t empt to solve this p roblem. Even this app roach requi res care to m a k e it specific~ for example , ana lys is of fish muscle, as opposed to pe rhaps v iscera or gills, is u n l i k e l y to show whe the r a fish has b e e n exposed to h igh levels of Zn or Cu.

In Res t ronguet C r e e k it was r easonab le to assume that eco log ica l effects were r e l a t ed to meta l s bu t imposs ib le from ana lyses and s imple toxici ty tests a lone to speci fy wi th any cer ta in ty whe the r Cu or Zn was most important . However , the s tudy i l lus t ra ted in F igure 3 demons t ra tes the d e v e l o p m e n t of a very m a r k e d di f ference b e t w e e n the to le rance to Cu of Fucus from the C r e e k and that of other popula t ions : the di f ference for Zn was much less obvious, i nd ica t ing that Cu had the more impor tan t impac t on this species . Luoma (1977) has advoca t ed the s tudy of d i f ferences in to le rance b e t w e e n normal and po l lu t ed popu la t ions towards specif ic toxins as a means of iden t i fy ing which con taminan ts are hav ing most impact . Al l i nduc ib le to le rance mechan i sms (e. g. meta l lo th ioneins) m a y not be comple t e ly me ta l specif ic but to le rance hav ing a gene t i c bas is is usua l ly (but not a lways) specif ic (cf. Bryan, 1976; Brown, 1978).

Var ious s tudies fo l lowing the rec iprocal t ransfer of organisms b e t w e e n uncon tami - na t ed and con tamina ted a reas have p roved useful in assess ing effects. For example , changes in me ta l r e s idue levels and condition- in t ransfer red Scrobicularia plana were used to assess wha t had a p p e a r e d to be a de le te r ious effect of Pb and other meta ls (Bryan & Hummers tone , 1978). Concen t ra t ion g rad ien t s in the f ie ld often provide su i tab le condi t ions for s tudies r e l a t ing effects to env i ronmen ta l levels~ for example , Shore et al. (1975) showed that there was a poss ib le corre la t ion b e t w e e n inc reas ing levels of Cd in the l impe t Patella vulgata a long the Severn Estuary - Bristol Cha nne l and r e d u c e d ab i l i ty to u t i l ize g lucose (cf. Tab le 5).

The use of b ioassays to assess wa te r qual i ty is normal ly non-specif ic . However , wi th the hydro id Campanularia flexuosa the inf luence of meta l s in wa te r of low qual i ty from the Bristol Channe l was m e a s u r e d b y the improvemen t obse rved w h e n they were r emoved from the wa te r wi th Che lex res in {Stebbing, 1979). Other s tudies in the same sea a rea have demons t r a t ed the occurrence of de le te r ious effects in musse ls as infer red by var ious phys io log ica l and b iochemica l ind ices of condi t ion (cf. Bayne et al., 1979) and the h igh inc idence of d i s ea sed spec imens (Lowe & Moore, 1979). At p resen t these s tudies are l a rge ly unspecif ic , but a t tempts are b e i n g m a d e to arr ive at ind ices that migh t measu re the effects of s ingle c lasses of pol lu tant .

Heavy-meta l con tamina t ion in the sea 21

Effects o n m a m m a l s a n d m a n

Genera l ly speaking, there is little ev idence for the deleter ious effects of heavy metals on mar ine mammals . However, S toneburner (1978) has suggested that Hg may have caused the s t randing of pilot whales based on the observat ion that Hg. Se ratios in the livers of some whales far exceeded the 1:1 molar ratio usual ly observed: this normal ly seems to result from the storage of Hg as mercuric se lenide granules fol lowing the demethyla t ion of methyl Hg absorbed from the fish diet (Martoja & Viale, 1977). It has b e e n observed that Hg levels in the livers of seals t end to increase with age, par t icular ly in con tamina ted areas, whereas concentrat ions in muscle remain low. Roberts et al. (1976) observed about 1 ppm (wet) in muscle from the common seal Phoca vitulina compared with more than 100 ppm in the liver of the oldest animals.

Studies on nat ives of the C a n a d i a n Arctic who eat seals have shown them to have somewhat increased levels of Hg in hair and blood but no evidence of poisoning has b e e n discovered (cf. Smith & Armstrong, 1978). As far as I am aware, with the except ion of Minamata disease there is no evidence that mar ine foodstuffs have caused any pe rmanen t form of metal poisoning in humans . However, the dietary in take rates of metals such as Hg and Cd regarded as tolerable are so low that they can readi ly be exceeded by ea t ing con tamina ted seafood (cf. FAO/WHO, 1972).

A b a t e m e n t of c o n t a m i n a t i o n

Fujiki (1973) reported that whereas in 1959 the bivalve Venus japonica from Minamata Bay conta ined 178 ppm (dry) of Hg this had fal len to only a few ppm in 1970 fol lowing removal of the Hg sources. However, levels of Hg in the sediments r ema in as h igh as 100 ppm at some sites and are gradual ly be i ng dispersed to other areas (Kumagai & Nishimura, 1978). Fol lowing a reduct ion of 95-98 % in the Hg output from an I ta l ian chlor-alkali p lan t it was observed that in 28-29 months the concentra t ion in the crab Pachygrapsus marmoratus fell by 78 % and the fall in other species r anged from 2 0 - 3 1 % (Renzoni, 1976). It was noted that complete recovery would probably be de layed by the large amounts of Hg bui l t up in the sediments . Of course, it is not always so easy to stop the inpu t of wastes. For example, examina t ion of a dated sed iment core from the Tamar Estuary by Clifton & Hami l ton (1979) showed that levels of Cu, Zn and Pb in the sediments rose sharply fol lowing a peak of metal l i ferous m i n i n g in the mid -n ine t een th century and have r ema ined constant for the past 100 years. This has b e e n caused by cont inua l input from the wea ther ing of spoil heaps and, a l though the estuary is regarded as unpol lu ted, concentrat ions of metals in the biota are abnormal ly high.

Acknowledgement. Some of the work described in this paper was supported by the Department of the Environment under Contract DGR 480/51.

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