8/8/2019 Dal Linger

1/8

Oecologia (Berlin) (1987) 73:91-98 Oecologia9 Springer-Verlag 1987

C o n t a m i n a te d f o o d a n d u p t a k e o f h e a v y m e t a l s b y f is h :a r e v i e w a n d a p r o p o s a l f o r f u r t h e r r e s e a r c hR . D a l l i n g e r 1 , F . P r o s i 2 , H . S e g n e r 3 , an d H . B a c k 31 Institu t ffir Zoologic (A bteilung Zoop hysiologie), TechnikerstraBe 25, A-6020 Innsbruck, Austria2 Institu t ffir Zoologic I (Morphologie/{Jkologie), Im N euenheimer Fold 230, D-6900 Heidelberg,Federal Republic of Ge rma ny3 Anatomisches Insti tut III der U niversitS.t , Im Neuenheimer Fold 307, D-6900 Heidelberg, Federal Republic of Ge rm any

S u m m a r y . 1 . T h e u p t a k e o f h e a v y m e t a l s v i a t h e a l i m e n t a r yt r a c t c a n b e a n i m p o r t a n t f a c t o r f o r t h e m e t a l b u d g e t o ff i s h . 2 . C o n c e p t s s u c h a s b i o m a g n i f i c a t i o n , b i o a c c u m u l a -t i o n , b io t r an s fe ren ce , o r co n cen t r a t i o n f ac to r s , co n v ey l i t t l ei n f o r m a t i o n a b o u t t h e r e a l t h r e a t o r i g i n a t i n g f r o m h e a v ym e t a l s i n a n a q u a t i c f o o d c h a i n . 3 . I n p o l l u t e d a q u a t i c e c o -s y s t e m s th e t r a n s f e r o f m e t a l s t h r o u g h f o o d c h a i n s c a n b eh i g h e n o u g h t o b r i n g a b o u t h a r m f u l c o n c e n t r a t i o n s i n t h et i s su es o f fi sh . Th i s r e l a t i o n sh ip i s ca l led t h e fo o d c h a inef f ec t. 4. Tw o k in d s o f eco lo g i ca l f ac to r s i n f l u en ce t h e fo o dch a in e f f ec t : f ir s t l y , h ig h l ev e l s o f co n t a m in a t i o n o f t h efo o d , an d , s eco n d ly , t h e r ed u c t i o n o f spec i es d iv e r s i ty .W h e n s u s c e p t i b l e s p e c i e s a r e e l i m i n a t e d , m e t a l - t o l e r a n tf o o d o r g a n i sm s m a y b e c o m e d o m i n a n t . T h e i r to l e r a nc em a y b e b a s e d e i t h e r o n t h e i r a b i li t y to a c c u m u l a t e e x c e ss i vea m o u n t s o f m e t a ls o r t o e x c l u de h e a v y m e t a l s f r o m t h et is s u es . T h e s e t w o s t r a t e g ie s r e p r e s e n t f e e d b a c k m e c h a n i s m sw h i c h m a y e n h a n c e o r w e a k e n t h e f o o d c h a i n e f f e c t . 5 .I t i s c o n c l u d e d t h a t f u t u r e i n v e s t i g a t i o n s o n t r a n s f e r e n c eo f h e a v y m e t a l s t o f i sh m u s t t a k e i n t o m o r e c a r e f u l c o n s id -e ra t i o n t h e sp ec i f i c eco lo g i ca l s i t u a t i o n o f a g iv en en v i ro n -m e n t .K e y w o r d s : F i s h - F o o d - H e a v y m e t a l - F o o d c h a i n e f f e c t

M a n y f is h s p e c ie s a r e a m o n g t h e t o p c o n s u m e r s o f tr o p h i cp y r a m i d s i n a q u a t i c e c o s y s t e m s . I n c o n s e q u e n c e , t h e y a r ee n d a n g e r e d b y d i e t - b o r n e p o l l u t a n t s t r a n s f e r r e d a l o n g t h efo o d ch a in (S / i rk k / i e t a l . 1 9 7 8 ; M o r i a r t y 1 9 8 4 ) .T h e a c c u m u l a t io n o f h e a v y m e t a l s d e p e n ds o n u p t a k ev i a c o n t a m i n a t e d f o o d a n d v i a w a t e r , b u t t h e r e l a t i v e i m -p o r t a n c e o f th e s e t w o a v e n u e s f o r m e t a l u p t a k e o f t e n r e -m a i n s u n c e r t a i n . M o r e o v e r , t h e p o s s ib i l it y h a s t o b e c o n s i d -e r e d t h a t i n m a n y a q u a t i c e c o s y s t e m s t h e b i o a v a i l a b i li t yo f h e a v y m e t a l s m a y h a v e c h a n g e d d u r i n g t h e p a s t y e a r sd u e t o i n c r e a s i n g e f f o rt s in w a s t e w a t e r t r e a t m e n t ( J e r n e l 6 va n d L a n n 1 9 7 1 ; F 6 r s t n e r a n d M f i l l e r 1 9 7 4 ; W a c h s 1 9 8 1 ;M / i l l e r 1 9 83 ) o r b eca u se o f t h e es t ab l i sh m en t o f s tr i c t en v i -r o n m e n t a l s t a n d a r d s a n d l a w s w h i c h r e g u la t e e m i s s i o n s( C z a r n e z k i 1 98 5) . A s a c o n s e q u e n c e , t h e g r e a t e r p a r t o fh e a v y m e t a l s m a y n o w b e c o n t a i n e d i n p a r t i c u l a t e f r a c t i o n sb e c a u s e o f th e d e c r e a s e d c o n c e n t r a t i o n s o f w a t e r - b o r n ei o n ic c o m p o u n d s . T h i s s i t u a t i o n m a y l e a d to e l e v a t e d c o n -Offprint requests to. R. Dallinger

c e n t r a t i o n s o f h e a v y m e t a l s i n b e n th i c a n i m a l s a n d m p l a n t s(M cIn to sh e t a l. 1 9 7 8 ; Tess i e r e t a l . 1 9 84 ).B i o m a g n i f i c a t i o n o f p o l l u t a n t s i s a w e l l k n o w n p h e n o -n a e n on , e s p e c i a ll y w i t h r e s p e c t t o s o m e o r g a n i c c o m p o u n d s ,l ik e o r g a n o c h l o r i n e s o r p o l y c h l o r i n a t e d b i p h e n y l s ( J a r v i n e net al . 1977; Pa asi v i r t a et a l . 1983; P aa siv i r ta e t a l . 1985).F o r h e a v y m e t a l s , h o w e v e r , t h is a s s u m p t i o n i s th e s u b j e c to f c o n fl i c ti n g a r g u m e n t s , a n d , a s s t a t e d b y F e r a r d e t a l .( 1 9 8 3 ) , t h e t e r m b i o m a g n i f i c a t i o n h a s o f t e n b e e n m i s u s e d .Nev e r th e l es s , t i s su es o f m an y f i sh sp ec i es co n t a in e l ev a t edm e t a l c o n c e n t r a t i o n s e x c e e d i n g t h e n a t i o n a l l y o r i n t e r n a -t i o n a l l y a g r e e d q u a l i t y s t a n d a r d s f o r f i s h m e a t ( F 6 r s t n e ran d M f i l l e r 1 9 74 ; Na b rzy sk i 1 9 7 5 ; M i i l le r an d P ro s i 1 9 7 8 ;P h i l l i p s e t a l . 1 9 8 0 ; Czarn ezk i 1 9 8 5 ; Da l l i n g er an d Kau tzk y1985 a).

I n t h i s r e v ie w a n a t t e m p t i s m a d e t o e v a l u a t e t h e r e l a t iv ec o n t r i b u t i o n s o f w a t e r a n d f o o d t o m e t a l u p t a k e b y f is h .Th e ec o lo g i ca l s i g n i fi can ce o f wh a t i s ca ll ed t h e fo o d ch a inef f ec t i s p o in t e d o u t . I t i s co n c lu d ed t h a t f a c to r s i n f l u en c in gth i s e f f ec t sh o u ld b e su b j ec t ed t o mo re p rec i se a t t en t i o n .B ioava i lab il i ty o f me ta l s in w a te r and the pa thw ays o f t he i rup take by f i s hI n a q u a t i c s y s t e m s t he a v a i l a b i l i ty o f a m e t a l t o o r g a n i s m sd e p e n d s o n m a n y p h y s i c o - c h e m i c a l a s w e l l a s b i o l o g i c a lf a c t o r s ( se e F 6 r s t n e r a n d W i t t m a n n 1 98 1 ; H ~ k a n s o n 1 98 4) .Av a i l ab i l i t y i s i n f l u en ced , fo r i n s t an ce , b y t h e ch emica l sp e -c l a r i o n o f io n i c r ect a1 fo rm s , f l~e ch e mis t ry o f w a t e r a n dt h e r e l a ti v e d i s t ri b u t i o n o f m e t a l s b e t w e e n s o l u b le a n d p a r t i -c u l a t e f r a c ti o n s . T h e s p e c i a t i o n o f a m e t a l i n a q u e o u s s o l u -t i o n s d e p e n d s o n t h e n u m b e r a n d p r o p e r t i e s o f i o n i c s pe c ie sa n d b i n d i n g s t a t e s ( S t u m m a n d K e l l e r 19 84 ). B a s i c p r o b -l e m s o f m e t a l s p e c i a t io n i n s e a w a t e r h a v e b e e n d i s c u s se db y M i l l e ro (1 9 7 7 ) an d Ke s t e r e t a l . ( 19 8 6 ). I t h as b ee ns h o w n , m o r e o v e r , t h a t t h e u p t a k e a s w e l l a s t h e t o x i c i t yo f h e a v y m e t a l s m a y s u b s t a n t i a l l y d e p e n d o n t h e c h e m i c a lsp ec i es i n v o lv ed (S u n d a an d Gu i l l a rd 1 9 7 6 ; Giesy e t a l .1 9 77 ; S u n d a e t a l. 1 9 7 8 ; A m i a r d - T r i q u e t a n d S a a s 1 9 7 9 ;C h a k o u m a k o s e t a l. 1 97 9; C z u b a a n d M o r t i m e r 1 98 0; V a nd er P n t t e e t a l . 1 9 81 ; Bo rg m an n 1 9 8 3 ; M i ll s 1 9 8 6; P i sca to r1986).

T h e c h e m i s t r y o f w a t e r i t s e lf in f l ue n c e s t h e s p e c i a t i o no f h e a v y m e t a l s i n b o t h m a r i n e a n d l i m n i c e n v i r o n m e n t s .F a c t o r s s u c h a s h y d r o g e n i o n a c t i v i t y (H g t k a n s o n 1 9 80 ; B a -c i n i a n d S u t e r 1 9 7 9 ) , h a r d n e s s ( K i n k a d e a n d E r m a n 1 9 7 5 ;Be ll 1 9 7 6 ; M c Ca r ty e t a l . 1 9 7 8 ; Ca l a ma r i e t a l . 1 98 0) , an d

8/8/2019 Dal Linger

2/8

92salinity (Somero et al. 1977), are reported to be crucial inthis respect. Furthermore, the presence of organic com-pounds and suspended particles may change the activityof free metal ions (Brown et al. 1974; Ramamoorthy andKushner 1975; Gfichter and Davis 1978; Hirose and Sugi-mura 1985; Bernhard and George 1986). Binding to, andreleasing from sediment (Gardiner 1974; Patrick et al. 1977;Sakata 1985) also affects the availability of metals to aquat-ic life (Franc is et al. 1984; Tessier et al. 1984; Prosi a ndMiiller 1987), as do biological or chemical transformations,such as the methylation of mercury (Jensen and Jernel6v1969).Among the biological factors affecting metal availabili-ty, species specific differences like feeding behaviour (Phil-lips et al. 1980; Van Hassel et al. 1980; Bernhard and An-dreae 1984; Willis and Sunda 1984; Czarnezki 1985; Loringand Prosi 1986) and habitat preferences (Delisle et al. 1975;Ney and Van Hassel 1983) play a dominant role. Thesebasic features are modified by physiological factors, suchas accumulati on rates and the binding capacity in an animal(Pentreath 1977; Jeng and Sun 1981), as well as by ecologi-cal influences like temperature (Somero et al. 1977; Edgrenand Notter 1980; Prosi and Mfiller 1987) and feeding habits(Manthey et al. 1979; Mathers and Johansen 1985).As a consequence, the pathways of metal flux intoaquatic organisms depend on specific features of waterchemistry, sediments, and on the biological characteristicsof the organisms. As far as fish are concerned, there arethree possible ways by which metals may enter the body:the body surface, the gills, and the alimentary tract.Little is known about the uptake of heavy metalsthrough the skin. It can be assumed, however, that thebody surface of fish is more or less impervious to harmfulsubstances in the sur rounding water. There are some indica-tions that mucus secretion may prevent heavy metals fromentering the body of fish (Varanasi and Marke y 1978; Lockand Van Overbeeke 1981 ; Eddy and Fraser 1982; Pfirt andLock 1983).

The assumption that the skin does not play a dominantrole in the uptake of heavy metals is not true for the gills:They are not only the main organs of gas exchange, but,as a highly specialized and exposed part of the body surface,also represent an important site of uptake of essential andnon-essential metal ions from the water (Chartier 1974;Fenwick and So 1974). For instance, after exposure of fishto soluble zinc or cadmium these metals are found in theirgills (Hughes and Flos 1978; Westernhagen et al. 1978).It has been shown by P/irt and Svanberg (1981) that cadmi-um is taken up by perfused gills of rainbow trout, a signifi-cant uptake occurring immediately after exposure (Ander-son and Spear 1980; Collvin 1984; Segner 1987). Fromthe gills, the absorbed metals are distributed throughoutthe whole body and accumulate in specific organs. Heavymetals have also been reported to induce harmful changesin gill morphology (Haider 1964; Baker 1969; Skidmore1970; Van der Putte et al. 1981; Karl sson-N orrgre n et al.1985). It thus seems that passage through the gills is animpor tant pathw ay for the soluble fractions of heavy metalsinto fish.Uptake of particulate metal fractions by fish occurs,if at all, from contaminated suspended matter, sediments,and organisms serving as food sources, the only feasibleroute being the alimentary tract. In many aquatic systemspollution has led to metal contamination of the food organ-

Table 1. Estimated or quantified (in brackets) relative contributionsof food and water to the accumulation of heavy metals in freshwater fish species. Heavy metals, fish species, relative contributionsof food and water, and references are specified. Explanation ofsigns: + +. . . dominance of one pathway over the other. + .. .a positive contribution to metal uptake has been observedHeavy metal Fish species Contribution to Referencemetal uptake from

Food WaterCdCo-60CuMethyl-Hg

Pb

Zn

Gambusia affinis + + + aSalmo gairdneri + + (?) bCyprinus carpio + + + cSalmo gairdneri + + + (?) bSalmo gairdneri + + dEsox lucius + + (60%?) +Perca flavescens + + (60%?) +Salmo gairdneri - + +Salmo gairdneri + + (?) bPoeciliareticulata + + +Salmo gairdneri + + + (?) bRutilus rutilus + + + (?) i

Williams and Giesy 1978; b Dallinger and Kautzky t985;Amiard and Amiard-Triquet 1979; d Phillips and Buhler 1978;Jernel6v and Lann 1971; f Norstr6m et al. 1976; g Hodson et al.1978; h Vighi 1981 ; i Yediler 1978

isms of various fish species (Mathis an d Cumm ings 1973;Hardisty et al. 1974; Prosi 1977; Anderson et al. 1978; Spe-har et al. 1978; Heyr aud and Cherry 1979; Prosiet al. 1979;Van Hassel et al. 1980). Moreover, metal-containing foodrepresents a much more highly contaminated source thanwater, in which the concentrations, even from highly pol-luted sites in the field, are lower. Food may therefore bean impor tant source of metal contam ination in fish. Al-though most of the work supporting this view is based onlaboratory experiments (Hoss 1964; Saward et al. 1975; Pa-trick and Lou tit 1976; Ao ya ma et al. 1978; Jacobs 1978;Patrick and Loutit 1978; Amiard-Triquet 1979; Amiardand Amiard-Triquet 1979; Hamdy and Prabhu 1979; Jengand Sun 1981; Vighi 1981; Murai et al. 1981; Knox et al.1982; Milner 1982; Tarifeno-Silva et al. 1982; Ferard et al.1983; Segner and Back 1985), in a few instances the prob-lem has been studied in the field (Dallinger and Kautzky1985 b). It thus appears that gills and gut are both importantpathways for metal upta ke in fish (Kumada et al. 1973;Bernhard and Andreae 1984; Willis and Sunda 1984): Solu-ble metal fractions may accumulate preferentially via thegills, particulate metal fractions via the alimentary tract.The relative importance of ood as a source of heavy metalsIn only few studies has an attempt been made to quantifyor at least estimate the relative contributions of water andfood to metal uptake by fish. Tables 1 and 2 summarizesome results of such studies for fresh water (Table 1) andmarine fish species (Table 2). Most of the data are derivedfrom laboratory experiments, in some cases employing ra-dioactive nuclides. In situations in which fish are allowedto take up heavy metals simultaneously from both waterand food the latter pathway generally dominates. This is

8/8/2019 Dal Linger

3/8

Table 2. Estimated or quantified (in brackets) relative contribut ionsof food and water to the accumulation of heavy metals in marinefish species. Heavy metals, fish species, relative contr ibut ions offood and water, and references are specified. Explanat ion of signs :+ + ... dominance of one pathway over the other. + ... a positivecontribution to metal uptake has been observedHeavy metal Fish species Contribution to Referencemetal uptake from

Food WaterCd-115

Mn-54Zn-65

Zn

Pleuronectesplatessa + + + aRaja clavat" + + + "Pleuronectesplatessa + + + bPleuronectesplatessa + + + bParalychthys sp. + + (65%) + ~Pleuronectesplatessa + + +(10%) d

Gambusiaaffinis + + (78%) +Leiostomusxanthurus + + (82%) + eGobius sp. + + (60%) + e

a Pentreath 1977; b Pentreath 1973; c Hoss 1964; d Milner 1982;e Willis and Sunda 1984; f Renfro et al. 1975

best documented for zinc, the rapid assimilation of whichmay be due to its role as an essential trace element. Highlytoxic elements like lead and cadmium are also assimilatedfi'om food, cadmi um appare ntly more ra pidly in freshwaterthan in marine habitats. As far as mercury is concerned,most observations have involved the methylated metal.Lock (1975) observed that in Salmo gairdneri the uptakerate of methylmercury from water was higher than fromthe food, but the percentage uptake of the metal from thelatter source was 5-10 times higher. Contradictory results

93have been reported for lead (compare Hodson et al. 1978;Vighi 1981), but the reality of the food pathway cannotbe denied. It remains to be seen to what extent laboratoryfindings reflect the actual situations in the field. In laborat o-ry experiments the food offered to the fish is, as a rule,uniforml y conta minat ed with heavy metals; this is certainlynot true for most polluted habitats in nature, where fishare able to choose between different kinds of food. Thusin the field food may be a less important source of heavymetals than in the laboratory, but its role should not beunderestimate d (Dallinger and Kaut zky 1985 b).

The uptake of heavy metals from food depends on var-ious influences. Some reports i ndicat e that a signi ficant ab-sorption of a metal by fish takes place only, if the metalcontent in the food exceeds a min imu m threshold level (Ja-cobs 1978; Murai et al. 1981). Moreover, feeding frequencyand co nsumt pion rates (Aoya ma et al. 1978; Mathers a ndJohansen 1985), diet quality (Renfro et al. 1975), and inter-actions with water-borne metals may modify food-relatedmetal acc umulat ion in fish.

An important question is whether the extent of metaluptake from water or food is reflected in elevated concen-trations of different organs. For instance, after contamina-tion with copper or cadmiu m high metal contents are foundin liver and kidney (Mfiller and Prosi 1978; Edgren andNotter 1980; Wachs 1982; Dallinger and Ka utzk y 1985b).Since these organs are targets fo r final depositi on of variousheavy metals, the levels in both organs seem to be indepen-dent of the pathwa y of uptake. However, it is to be expectedthat the cont ributi ons of water and food to metal uptakein whole fish are reflected by high co ncen trat ions in gillsand gut tissue, respectively. Table 3 summarizes some re-suits compari ng the concentra tions of different tissues frommarine and freshwater fishes contaminated via water andvia food. In fishes taking up heavy metals from water (Tab-le 3 a), the gills generally show higher c once ntr atio ns thangut tissues or other organs. On the other hand, fish accumu-lating heavy metals from food (Table 3b) show elevatedmetal levels in the gut compared to gills or other organs.Both gills and gut are probably sites of transient metal

Table 3. Compar ison of metal concentrations in different tissues of fish according to uptake by water and by food. Metals, fish species,organs and references are specified. The concent rations in organs are not quantified, but ranked in decreasing orderHeavy metal Fish species Tissue or organ, ranked by concentration Referencea accumula tion by waterCd-115 Pleuronectes platessaRaja clavataCd Pleuronectes platessaPerca fluviatilisCo-60 Cyprinus carpioMn-54 Pleuronectes platessaZn-65 Pleuronectes platessab accumula tion by foodCd Salmo gairdneriCo-60 Cyprinus carpioCu Salmo gairdneriHg Cichlasoma facetumZn Cyprinus carpioSalmo gairdneri

gill filaments > intestine> livergill filaments > liver > intest inegills > liver > muscle bgills > gut ~gills > digestive tract dgills > gut egills > kidney > liver > gut e

intestine > liver rdigestive tract > gills dliver > intest ine rgut > liver > muscle > head gdigestive tract > kidney > hepatopancreas > spleen > skin and muscle hgut tissue > gills i" Pentreath 1977; b Westernhagen et al. 1978; c Edgren and Notter 1980; a Amiard and Amiard-Trique t 1979; e Pentreath 1973;f Segner and Back 1985; g Hamdy and Prabhu 1979; h Jeng and Sun 1981; i Dallinger and Kautzky 1985b

8/8/2019 Dal Linger

4/8

94Table 4. Explanation of formal relationships referring to the uptakeof heavy metals by fish. Concepts, definitions, and formulas arereportedConcept Definition FormulaBiomagnification

Biotransference

Biotransference factor

Bioaccumulation

Concentration factor

Metal levels increaseprogressively along the trophicpyramidTransfer of heavy metalsthrough successive linksof a food chain C~Concentration of a metal in TI -an organism in relation tothe next lower trophic linkof a food chain.Heavy metals in biota areconcentrated in relation toabiotic environmental levels C,cMetal concentration within C j - Ceatrophic component inrelation to abioticenvironmental levels

Explanation of symbols : T transference factor; C~ metal concen-tration in atrophic level x; Cx_l metal concentration in the nextlower trophic level x-1 ; C concentration factor; Ctc metal concen-tration in a trophic component; Cemetal concentration of abioticenvironment

accumulation, their concentrations depending, among otherfactors, on the transfer rates at which absorbed metals arecarried to the final target sites in fish.The role of aquatic food chains in metal toxicityand accumulation in fishIn order to describe the transfer of heavy metals throughaquatic f ood chains terms like ~ biomag nific ation" , ~ bioac-cumulation", or "concentration factors", have been intro-duced. Unfortunately, the terms have often been misused(Ferard et al. 1983) or carelessely adopted.In Table 4 the concepts behind the terms are su mma-rized and defined (Vinikour et al. 1980; Vighi 1981 ; Wachs1981 ; Ferard et al. 1983; Dallinger 1986).Biomagn~'cation means that metals are progressivelyconcentrated within a given food chain, metal levels increas-ing with the order o f the trophic level. Whether biomagnifi-cation of heavy metals occurs in fish is a controversial ques-tion. The hypothesis is supported by some authors (Gold-water 1971 ; Peakall and Lovett 1972), but rejected by mostothers (Leland and McNurney 1974; Giesy and Wiener1977; Wiener and Giesy 1979; Prosi et al. 1979; MeFarlaneand Franzin 1980; Wachs 1981). Experimental evidenceagainst biomagnification has been presented in several stu-dies (Knauer and Martin 1972; Amiard-Triquet 1979;Gfichter and Geiger 1979; Hamdy and Prabhu 1979).Biotransference is defined as the relative enrichment ofheavy metals th rough successive links o f food chains. Bioac-cumulation means that heavy metals in organisms are con-centrated in relation to abiotic environmental levels, suchas those o f water or sediment. Concentration actors indicatehow many times a fish concentrates a metal above a certainenvironmental level which is usually (but not always !) that

of water. Similarly, biotransferencefactors express the con-centration of a metal in an organism in relation to thenext lower trophic level. Several problems are inherent tothese concepts. For instance, the values of bioconcentrationand biotransference factors change according to the envi-ronmental medium or food type chosen as reference. Thiscan be a proble m wherever the primary source of metalsand their pathways through food chains are not exactlyknown. Bioconcentration and biotransference factors ex-press, in these cases, fictive magnitudes. They are, more-over, inappropriate variables for considering and estimatingharmf ul levels o f a given metal within the tissues of a fish.

It has been found that both bioconcentration and bio-transference factors can (but need not) increase along agiven food chain up to the level of the organisms on whichthe fish species feed (Heyraud and Cherry 1979; Bernhardand Andreae 1984; Dallinger and Kautzky 1985b; Dall-inger 1986). On the trophic level of fish, however, thesefactors are usually reported to decrease again (Enk andMathis 1977; Amiard-Triquet 1979; Amiard-Triquet andSaas 1979; Gfichter and Geiger 1979; Mathis et al. 1979;Vighi 1981 ; Tarefeno-Silva et al. 1982; Fe rard et al. 1983 ;Bernhard and Andreae 1984). One reason for this is thatheavy metals are more available to orga nism of lower- thanto those of higher trophic levels. Moreover, fish seem tobe able to reject large amounts of the heavy metals ingested(Ha mdy and Pra bhu 1979; Tarifeno-Silva et al. 1982). Asmentioned above, this may be true to a greater extent fornon-essential and more toxic elements than for essentialones. In addition, the comparison of concentration factorsalong a food chain may give an inaccurate description ofthe actual metal transfer, since fish concentrate heavy met-als in certain organs which make only a small contributionto the total body weight. For a real estimate for the metalinput rate from food such factors as the total amount offood consumed and the faecal loss of heavy metals haveto be known (Milner 1982).The findings that bioconcentration and biotransferencefactors decrease at the level of the fish should not obscurethe fact, however, that transfer of heavy metals throughfood chains remains an important issue in metal assimila-tion by fish. Most heavy metals are effective at very lowconcentrations, so even low assimilation rates (reflected bysmall transfer factors) are sufficient to attain biologicallysignificant or harmful concentrations in tissues (Jackimet al. 1970; Murai e t al. 1981 ; Segner and Back 1985).Ecological constraints and the food chain effect." possibleconnections and feedback mechanismsThe concepts of "biomagnification" and "bioconcentra-tion" convey little information regarding the real threatfrom heavy metals in an aquatic food chain. Even if bio-magnification is not observed, or bioconcentration factorsare small, the amount of metal transferred via food canbe high enough to reach harmful levels in the tissues o faquatic animals, endangering the animals themselves as wellas possible predators or consumers (Eisler et al. 1972). Weshall refer to this relationship as the food chain effect.An important question concerns the extent to whichthe f ood chain effect in fish may be influenced by ecologicalconditions. Two possible factors should be considered.The first of these is related to the degree of contamina-tion of the food supply. It has been shown that heavy metal

8/8/2019 Dal Linger

5/8

95p o l l u t i o n i n a q u a t i c e c o s y s t e m s i s o f t e n m o r e m a r k e d l y r e -f l e ct e d b y h i g h m e t a l l e v el s i n s e d i m e n ts , m a c r o p h y t e s a n db e n t h i c a n i m a l s t h a n b y e le v a t e d c o n c e n t r a t i o n s i n w a t e r( M a t h i s a n d K e v e r n 1 9 7 5 ; E n k a n d M a t h i s 1 9 7 7 ; M c I n t o s he t a l . 1 9 7 8 ; M a t h i s e t a l. 1 9 7 9 ; P r o s i e t a l. 1 9 7 9 ; A b o - R a d y1 9 8 0 ; V a n H a s s e l e t a l . 1 9 8 0 ; P r o s i 1 9 8 1 ). T h i s p a t t e r n o fd i s t r i b u t io n m a y o c c u r w i t h b o t h l o w - a n d h i g h -l e v e l c h r o n -i c p o l l u ti o n ( D a l l in g e r a n d K a u t z k y 1 9 8 5 b) . D e p e n d i n g o nt h e i r h a b i t a t p r e f e r e n c e s o r s p e c i a l i z e d f o o d r e q u i r e m e n t sf is h m a y b e e n d a n g e r e d i n s u c h s i t u a ti o n s . I t h a s b e e ns h o w n , f o r i n s ta n c e , t h a t b o t t o m - d w e l l i n g f is h s p ec i es a c c u -m u l a t e h e a v y m e t a l s b e c a u s e o f th e i r a s s o c i a t io n w i t h m e t -a l - c o n t a i n i n g s e d i m e n t s ( D e l i sl e e t a l. 1 9 7 7 ; N e y a n d V a nH a s s e l 1 9 8 3 ). I n g e s t i o n o f s e d i m e n t a n d o f s e d i m e n t -d w e l l -i n g i n v e r t e b r a te s m a y b e a n i m p o r t a n t s o u r c e o f m e t a l u p -t a k e b y t h e s e fi s he s ( C z a r n e z k i 1 9 8 5 ; L o r i n g a n d P r o s i1 9 8 6 ) . I t i s l i k e l y t h a t t h e f o o d c h a i n e f f e c t i s e n h a n c e di n t h o s e a q u a t i c e n v i r o n m e n t s i n w h i c h m e t a l l o a d e d f o o d ,s u c h a s m a c r o p h y t e s o r i n v e r te b r a t e s , r e p r e s e n t a l a r g es h a r e o f t h e d ie t o f f i s h ( H a r d i s t y e t al . 1 9 7 4 ; M u r p h y e t a l.1978) .

A s e c o n d k i n d o f i n f lu e n c e o n t h e f o o d c h a i n e f f ec ti n f is h m a y b e d u e t o t h e r e d u c t i o n o f s p e ci e s d iv e r si t y.S e v e r a l a u t h o r s h a v e s h o w n t h a t h e a v y m e t a l p o l l u t i o n c a nl e a d t o t h e e l i m i n a t i o n o f s u s c e p t ib l e s p e c i e s ( B u r m e i s t e r1 9 8 0 ; R y g g 1 9 8 5 ; R o c h e t a l . 1 98 5 ) , t h u s i n c r e a s i n g t h ed o m i n a n c e o f a f e w t o l e r a n t a n d o p p o r t u n i s t i c s p e c ie s( L a n g a n d L a n g - D o b l e r 1 9 7 9 ). A s a c o n s e q u e n c e , t r o p h i cr e l a t io n s h i p s a r e s i m p l if i e d : f o o d c h a i n s a r e s h o r t e n e d a n dp r e d a t o r y f i s h a r e f o r c e d t o f e e d m o r e a n d m o r e o n a f e w ,o r e v e n o n l y o n e k i n d o f , m e t a l - t o l e r a n t f o o d o r g a n i s m s( D a l l i n g e r a n d K a u t z k y 1 9 8 5 b ) . M e t a l t o l e r a n c e o f f o o do r g a n i s m s i s b a s e d o n t w o o p p o s i t e e f f e c t s : d e t o x i f i c a t i o no f m e t al s b y c e l l u la r i n c l u si o n o n t h e o n e h a n d , a n d m e t a le x c l u s i o n o n t h e o t h e r .

A m o n g m e t a l - d e t o x i f y i n g f o o d o r g a n i s m s a q u a t i ci s o p o d s , s n a il s, a n d s l u d g e w o r m s a r e c a p a b l e o f s t o r i n gp a r t ic u l a r ly l a rg e a m o u n t s o f h e a v y m e t al s ( E n k a n d M a -t h i s 1 9 7 7 ; M 6 1 1e r 1 9 7 8 ; M a t h i s e t a l . 1 9 7 9 ; D a l l i n g e r a n dK a u t z k y 1 9 8 5 b ; R a i n b o w 1 9 8 5 ; P r o s i a n d B a c k 1 9 8 5 ). T h er e a s o n f o r t h is is t h a t t h e s e g r o u p s o f a n i m a l s p o s s e s s e f f i -c i e n t d e t o x i f i c a t io n m e c h a n i s m s b y w h i c h h e a v y m e t a l s a r eb o u n d t o m e t a l - b i n d i n g p r o t e i n s o r s t o r e d i n c e l l u l a r s t r u c -t u r e s l i k e v a c u o l e s a n d l y s o s o m e s ( B r o w n 1 9 7 7 ; B r o w n1 9 78 ; P r o s i 1 9 83 ; S i m k is s a n d M a s o n 1 9 83 ; B o u q u e g n e a ue t al . 1 9 8 4 ; D a l l i n g e r a n d P r o s i 1 9 8 6 ) . T h e s e l e c t i o n o f s u c ht o l e r a n t s p e c ie s in p o l l u t e d h a b i t a t s r e p r e s e n t s a n i m p o r t a n tp o s i t iv e f e e d b a c k m e c h a n i s m b y w h i c h t h e f o o d c h a i n e f fe c ti s i n t ens i f i ed ( D a l l i nge r 1986) .

T h e r e a r e, h o w e v e r , a l s o e x a m p l e s i n w h i c h t h e o p p o s i t ee f fe c t i s r e p o r t e d : G / i c h t e r a n d G e i g e r ( 1 9 7 9 ) f o u n d t h a tm e t a l p o l l u ti o n o f a q u a ti c e n v i r o n m e n t s m a y f a v o u r t h eg r o w t h o f m e t a l- t o l er a n t p h y t o p l a n k t o n s p ec ie s t h a t a r ec h a r a c t e r i z e d b y a d e c r e a s e d u p t a k e o f h e a v y m e t a l s p e ru n i t o f b i o m a s s . I n t h i s c a s e t o l e r a n c e i s a c h i e v e d b y t h ee x l u s i o n o f h e a v y m e t a l s. T h e a u t h o r s s u g g e s t e d t h a t s u c ha n e g a t i v e f e e d b a c k m e c h a n i s m c o u l d p l a y a n i m p o r t a n tr o l e in e c o s y s t e m s b y r e d u c i n g t h e a v a i l ab i l it y o f m e t a l sf o r o r g a n i s m s b e l o n g i n g t o h i g h e r t r o p h i c l e v e l s . I n t h i sc a s e t h e f o o d c h a i n e f f e c t w o u l d b e w e a k e n e d .T h e c o n c l u s i o n f r o m s u c h o b s e r v a t i o n s i s t h a t f u t u r ei n v e s t i g a ti o n s o n t h e h a z a r d o f m e t a l p o l l u t i o n f o r f is hs h o u l d n o t s o m u c h d e a l w i t h f o r m a l r e l a t io n s h i p s , l i k ec o n c e n t r a t i o n f a c t o r s o r b i o m a g n i f i c a t i o n , b u t s h o u l d g i v e

m o r e c a r e f u l c o n s i d e r a t i o n t o t h e s p e c i f i c e c o l o g i c a l s i t u a -t i o n o f a g iv e n e n v i r o n m e n t . T h e e x c l u s iv e m e a s u r e m e n to f m e t a l c o n c e n t r a t i o n s i n f is h , fi s h f o o d a n d w a t e r , a n dt h e c a l c u l a ti o n o f c o n c e n t r a t i o n f a c t o r s c a n b e c o n f u s i n ga n d m a y l e a d t o c o n f l i c t i n g r e s u l t s w h i c h a r e d i f f i c u l t t oi n t e rp r e t . T h e t r a n s f e r o f m e t a ls f r o m f o o d t o f is h c a n b ee s t i m a t e d o n l y w h e n t h e c o m p o n e n t s o f t h e lo w e r t r o p h i cl e v e l a r e a n a l y z e d a n d t h e i r c o n t r i b u t i o n t o t h e f o o d o ff i s h i s e v a l u a t e d . I n o r d e r t o a c h i e v e t h i s e n d , i n v e s t i g a t i o n so n t h e g u t c o n t e n t o f fi s h a re n e c e s s a ry . I n s h o r t , f a c t o r si n f l u e n c i n g t h e f o o d c h a i n e f f e c t m u s t b e m o r e a c c u r a t e l yc o n s i d e r e d i n o r d e r t o a c h i e v e a n u n d e r s t a n d i n g o f th e p r o -c e ss e s a n d p r o b l e m s o f m e t a l t r a n s f e r t h r o u g h f o o d c h a i n si n t o t h e b o d y o f f is h .Acknowledgements. W e thank P ro f . W ol fgang W iese r and JoyWieser for reviewing the manuscr ipt . The work was suppor ted bythe "Fo nd s zur F6rde rung der wissenschaf t lichen Forsc hun g in()s ter re ich" , projects Nr . P5962B an d S-35/04.

Re f e r e n c e sA bo-R ady M D K (1980) M akrophy t i s che W asse rp f l auzen a l sBioin dikato ren ffir die Schwermetallbelastung der oberenLeine . A rch H ydro biol 89 (3) :387~404Am iard JC , Am iard-Tr ique t C (1979) Dis t r ibut ion o f cobal t 60in a mol lusc , a crus tacean and a f reshwater te leos t : Var ia t ionsas a funct ion of the source o f pol lu t ion and dur ing e l imination.Env i ron Po l l u t 20 :199-213Amiard-Tr iquet C (1979) Modal i tes de la contaminat ion de deuxchaines trophiques dulcaquicoles par le cobalt 60. Wat. Air SoilPoll 12 : 155-170Amiard-Tr iquet C , Saas A (1979) Modal i tes de la contaminat ionde deux chaines t rophiques dulcaquicoles par le cobal t 60. I I .Con tamina t ion s imul tanee des organismes par 1 ' eau e t la nour-r iture . Water , A ir and Soi l Pol lu t 12:14 1-153Anderson PD, Spear PA (1980) Copper pharmacokinet ics in f i shgills. I . Kinetics in pumpkinseed sunfish, Lepomis gibbosus, o f

di f ferent body s ize . Wa t Res 14:1101-110 5Anderson RV, Vinikour WS, Brower JE (1978) The dis t r ibut ionof cadmium, cop per , lead and z inc in the biota o f 2 f reshwatersites with different trace me tal inputs. Ho larc t Ec ol 1 : 377-3 84A oy am a I , I noue Y osh inobu , I noue Y or i t e ru (1978) Expe r im en ta ls tudy on the concen tra t ion process o f t race e lement thro ugha food chain f rom the viewpoint of nut r i t ion ecology. WarRes 12 (10): 831-8 36Bacini P, Suter U (1979) MEL IM EX , an exper imental heavy metalpollution study: Chemical speciation and biological availabili tyof copper in lake water . Schweiz Z Hy drol 41:2 91-3 0tBaker JTP (1969) His tological an d e lect ron microscopical observa-t ions in copper poison ing in the winter f lounder (Pseudopleuro-nectes americanus). J F i sh R es B d C an 26 :27854793Bel l AV (1976) Waste cont rols a t base metal mines . Environ SciTec hnol t 0 : 130-135Bernhard M , Andreae M O (1984) Tran spor t o f t race metals inmar ine food chains . In : Changing Metal Cycles and HumanHeal th , N r iagu JO (ed) Dah lem K onferenzen 1984, Spr inger,Berlin Heidelberg New York, pp 143-167Bernhard M, G eorge SG (1986) Impor tan ce of chemical speciesin uptake, loss, and toxicity of elements for ma rine organisms.In : T he im por t ance o f chem ica l " spec i a t i on" i n env i ronm en talprocesses , Bernh ard M , Br inckm an FE, S adler PJ (eds) DahlemK onfe renzen 1986, Springer, Berlin Heidelberg Ne w York ,pp 275-299Borgmann U (1983) Metal specia t ion and toxic i ty of f ree metalions to aquat ic b iota . In : Aq uat ic Toxicolog y, Nr iag u JO (ed)W i ley , N ew Y ork 1983 , pp 47 -72B ouquegneau JM , M ar to j a M , Truche t M (1984) H eavy m e ta ls torage in mar ine animals under var ious environmental condi-

8/8/2019 Dal Linger

6/8

96tions. In: Toxins, drugs, and pollutants in marine animals, Bolis(eds), Springer, Berlin Heidelberg New York, pp 147-160Brown BE (1977) Uptake of copper and lead by a metal tolerantisopod Asel lus meridianus . Rac. Freshwat Biol 7 (3):235-244Brown BE (1978) Lead detoxification by a copper-tolerant isopod.Nature 276:388Brown VM, Shaw TL, Shurben DG (1974) Aspects of water qualityand toxicity of copper to rainbow trout. Wat Res 8 : 797-803Burmeister E-G (1980) Die aquatische Makrofauna des BreinigerBerges unte r besonderer Berficksichtigung des Einflusses yonSchwermetallen auf das Arteninventar . Spixiana 3 (1): 5%90Calamari D, Marchetti R, Vailatie G (1980) Influence of waterhardness on cadmium toxicity to Salmo gai rdner i Richardson.Wat Res 14:1421-1426Canton JH, Slooff W (1982) Toxicity and accumulation studiesof cadmium (Cd2 +) with freshwater organisms of differenttrophic levels. Ecotoxicol Eni ron Saf 6:113-128Chakoumakos C, Russo RC, Thurston RV (1979) Toxicity of cop-per to cutthroat trout (Salmo c larkO under different conditionsof alkalinity, pH, and hardness. Environ Sci Technol 13:213-219Chartier MM (1974) Osmoregulation et proteine liant le calcium(CaBP) des muqueses intestinales et branchiales de la truitearc-en-ciel, Salmo gai rdner i . C r Acad Sci Paris (279(D):927-930

Collvin L (1984) Uptake of copper in the gills and liver of perch,PercaJTuviat i l is . Ecol Bull Stockholm 36:57-61Czarnezki JM (1985) Accumulation of lead in fish from Missouristreams impacted by lead mining. Bull Environm Contam Toxi-col 34:736-745Czuba M, Mortimer DC (1980) Stability of methylmercury andinorganic mercury in aquatic plants (Elodea densa) . Can J Bot58 (3): 316-320Dallinger R (1986) Schwermetalle in limnischen Nahrungsket ten.Ost Fischerei 39 (10):281-293Dallinger R, Kautzky H (1985a) The passage of Cu, Zn, Cd, andPb along a short food chain into the fish Salmo gai rdner i . IntConference of heavy metals in the Environment, Athens 1985.Conference proceedings, vol. 1, pp 694-696Dallinger R, Kautzky H (1985b) The importance of contaminatedfood for the uptake of heavy metals by rainbow trout ( S a l m ogairdneri) : A field study. Oecologia (Berlin) 67:8~89Dallinger R, Prosi F (1986) Fract ionati on and identification ofheavy metals in hepatopancreas of terrestrial isopods: evidenceof lysosomal accumulation and absence of cadmium-thionein.In : Velthuis HHW (ed), Third European Congress of Entomo-logy, Amsterdam, Nederlandse Entomologische Vereniging1986. Congress proceedings, Par t 2, p328Delisle CE, Hummel B, Wheeland KG (1975) Uptake of heavymetals from sediment by fish. In : TC Hutchinson (ed) : Interna-tional conference on heavy metals in the environment, Toronto ,Ontario 1975, p821Eddy F, Fraser JE (1982) Sialic acid and mucus production inrainbow trout (Salmo gai rdneri Richardson) in response to zincand seawater. Comp Biochem Physiol 73C, 357-359Edgren M, Notter M (1980) Cadmium uptake by fingerlings ofperch (Perca fluviatilis) studied by Cd-l15m at two differenttemperatures. Bull Env ironm Conta in Toxicol 24:647-651Eisler R, Zaroogian GE, Hennekey RJ (1972) Cadmium uptakeby marine organisms: J Fish Res Bd Canada 29:1367-1369Enk M, Mathis BJ (1977) Distribution of cadmium and lead ina stream ecosystem. Hydrobiologia 52 (2-3):153-158Fenwick JC, So YP (1974) A perfusion study of the effect of stan-niectomy on the net influx of calcium-45 across an isolatedeel gill. J exp Zool 188:125-131Ferard JF, Jouany JM, Truhaut R, Vasseur P (1983) Accumulationof cadmium in a freshwater food chain experimental model.Ecotoxic Environmen t Saf 7:43 52F6rstner U, Miiller G (1974) Schwermetalle in Flfissen und Seenals Ausdruck der Umweltverschmutzung. Springer, Berlin Hei-delberg New York, p 225

F6rstner U, Wittman GT W (1981) Metal pollution in the aquaticenvironment . Springer, Berlin Heidelberg New York, 2nd ed.p 486Francis PC, Birge WJ, Black JA (1984) Effects of cadmium-en-riched sediment on fish and amphibian embryo-larval stages.Ecotoxic Environm Saf 8 : 378-387G/ichter R, Davis JS (1978) Regulation of copper availabil ity tophytoplankton by macromolecules in Lake Water. Envir SciTechnol 12:1416 1421G/ichter R, Geiger W (1979) MELIMEX, an experimental heavymetal polution study: Behaviour of heavy metals in an aquaticfood chain. Schweiz Z Hydrol 41 (2):277-290Gardiner J (1974) The chemistry of cadmium in natural water.II. The adsorption of cadmium in river muds and naturallyoccuring solids. Wat Res 8:157-171Giesy JP, Wiener JG (1977) Frequency distributions of trace metalsin five freshwater fishes. Trans Am Fish Soc 106:393Giesy JP Jr, Leversee GJ, Williams DR (1977) Effects of naturallyoccurring aquatic organic fractions on cadmium toxicity to S i-mocephalus serrulatus (Daphnidae) and Gam busia af f inis (Poeci-liidae). Wat Res 11:1013-1020Goldwater LJ (1971) Mercury in the environment. Sci Am 224(5):15-21Haider G (1964) Zur Kenntnis von Schwermetallvergiftungen beiFischen I. Bleivergiftung bei Regenborgenforellen Salmo gai rd-ner i Rich.) und ihr Nachweis. Z angew Zool 51:347-368Hgtkanson L (1980) The quantitative impact of pH, bioproductionand Hg-contamination on the Hg-content of fish (pike). EnvPoll 18:285-304Hgtkanson L (1984) Metals in fish and sediments from the riverKolbficksan water system, Sweden. Arch Hydrobiol 101(3): 373 400Hamdy MK, Prabhu NV (1979) Behavior of mercury in biosys-terns. III. Biotransference of mercury through food chains. BullEnvironm Contam Toxicol 21 : 170-178Hardis ty MW, Huggins RJ, Kart ar S, Sainsbury M (1974) Ecologi-cal implications of heavy metal in fish from the Severn Estuary.Mar Poll Bull 5 : 12-15Heyraud M, Cherry RD (1979) Polonium-210 and lead-210 in mar-ine food chains. Mar Biol 52:227-236

Hirose K, Sugimura Y (1985) Role of metal-organic complexesin the marine envi ronment. Mar Chem 16:239-247Hodson PV, Blunt BR, Spry DJ (1978) Chronic toxicity of water-borne and dietary lead to rainbow trout (Salmo gai rdneri ) inlake Ontario water. Wi t Res 12:869-878Hoss DE (1964) Accumulation of zinc-65 by flounder of the genusParalychthys . Trans Am Fish Soc 93 : 364-368Hughes GM, Flos R (1978) Zinc content of the gills of rainbowtrout (S. gairdneri) after treatment with zinc solutions undernormoxic and hypoxic conditions. J Fish Biol 13:717-728Jackim E, Hamlin JM, Sonis S (1970) Effect of metal poisoningon five liver enzymes in the killyfish (Fundulus heterocl is tus) .J Fish Res Bd Can 27:383-390Jacobs G (1978) Uber Aufnahme und Anreicherung yon Schwer-metallsalzen (Hg, Cd) aus Futte rmit teln in Regenbogenforellen.I. Mitteilung. Z Tierphysiol, Tierern/ihr, Futte rmittelkd40: 274-284Jarvinen AW, Hoffman MJ, Thorslund TW (1977) Long-term toxiceffects of DDT food and water exposure on fathead minnows(Pimephales promelas) . J Fish Res Board Can 34:2089-2103Jeng SS, Sun LT (1981) Effects of dietary zinc levels on zinc concen-trat ions in tissues of common carp. J Nutrit ion 111 (1):134-140Jensen S, Jernel6v A (1969) Biological methylation of mercuryin aquatic organisms. Nature (London) 220:753-754Jernel6v A, Lann H (1971) Mercury accumulation in food chains.Oikos 22 : 403-406Karlsson-Norrgren L, Runn P, Haux C, F6rli n L (1985) Cadmium-induced changes in gill morphology of zebrafish, Brachydaniorer io (Hamilton-Buchanan),and rainbow trout, Salmo gai rdneriRichardson. J Fish Biol 27:81 95Kester DR, Andreae MO, Bernhard M, Branica M, Duinker J,

8/8/2019 Dal Linger

7/8

97George SG, Lurid W, Luoma SN, Tramier B, Velapoldie RA,Vestal ML (1986) Chemical species in marine and estuarinesystems. In: The importance of chemical "speciation" in envi-ronmental processes, Bernhard M, Brinckman FE, Sadler PJ(eds) Dahlem Konferenzen. Springer, Berlin Heidelberg NewYork, pp 275-299Kinkade ML, Erdman HE (1975) The influence of hardness com-ponents (Ca 2 + and Mg 2 +) in water on the uptake and con-centration of cadmium in a simulated freshwater ecosystem.Environ Res 10:308-313Knauer GA, Martin JH (1972) Mercury in a pelagic food chain.Limnol Oceanogr 17: 868-876Knox D, Cowey CB, Adron JW (1982) Effects of dietary copperand copper: zinc ratio on rainbow trout Salrno g airdneri. Aqua-culture 27:111-119Kumad a H, Ki mura S, Yokote M, Mat ida Y (1973) Acute andchronic toxicity, uptake and re tention of cadmium in freshwaterorganisms. Bull Freshwat Fish Res Lab 22:157-165Lang C, Lang-Dobl er B (1979) The chemical environment of tubifi-cid and lumbriculid worms according to the pollution level ofthe sediment. Hydrob iologia 65 (3):273-282Leland HV, McNurney J M (1974) Lead tr ansport in a river ecosys-tem. Proc. Int. Conf . Transp. Persist. Chem. Aquatic Ecosyst.,Ottawa, III, pp 17 23Lock RAC (1975) Uptake of methylmercury by aquatic organismsfrom water and food. In: Sublethal effects of toxic chemicalson aquatic animals, Kroeman JH, Striks JJT WH (eds) Elsevier,Amsterdam, pp 61-79Lock RAC , Van Overbeeke AP (1981) Effects of mercuric chlorideand methylmercuric chloride on mucus secretion in rainbowtrout (Sa lmo ga irdner i Richardson). Comp Biochem Physiol69C : 67-73Loring DH, Prosi F (1986) Cadmium and lead cycling betweenwater, sediment, and biota in an artificially contaminated mudflat on Borkum (FRG). Wat Sci Tech Vol 38, Plymouth,pp 131-139Manthey G, Br/igmann L, Berge H (1979) Zu Fragen der Kad-miumkontaminatio n in der Nahrungskette: Wasser - Plankton- Fisch in der Ostsee. In : Kadmium-Sympos ium. Wissenschaft-liche Beitr/ige der Friedrich Schiller Universitf it Jena. Jena 1979,pp 202-206Mathers RA, Johansen PH (1985) The effects of feeding ecologyon mercury accumulation in walleye (Stizostedion vitreum) andpike (Esox luc ius ) in Lake Simcoe. Can J Zool 63:2006-2012Mathis BJ, Cummings TF (1973) Selected metals in sediments,water, and biota in the Illinois River. J Wat Poll Contr Fed45:1573-1583Mathis BJ, Kevern NR (1975) Distribution of mercury, cadmium,lead and thallium in a eutrophic lake. Hydrobiol 46(2-3) : 207-222Mathis BJ, Cummings TF, Gower M, Taylor M, King C (1979)Dynamics of manganese, cadmium, and lead in experimentalpower plant ponds. Hydrobiologia 67 (3):197-206McCarty CS, Henry JAC, Houston AH (1978) Toxicity of cadmi-um to goldfisch Carassius auratus, in hard and soft water. JFish Res Bd Can 35:35-42

McFarlance GA, Franzin WG (1980) An enumeration of Cd, Cu,and Hg concentrations in livers of northern pike, Esox luc ius ,and white sucker, Catos tomus commerson i , from five lakes neara base metal smelter at Flin Flon, Manitoba. Can J Fish AquatSci 37 : 1573McIntosh AW, Shephard BK, Mayes RA, Atchison G J, NelsonDW (1978) Some aspects o f sediments di stribu tion and macro -phyte cycling of heavy metals in a contaminated lake. J Envir-ohm Qual 7 (3):301-305Millero FJ (1977) Thermodynamic models for the state of metalions in seawater. In : The Sea, Goldberg ED (eds), vol. 6, Wiley,New York, pp 653-693Mills CF (1986) The influence of chemical species on the absorp-tion and physiological utilization of trace elements from thediet or environment. In: The importance of chemical "specia-

tio n" in environmental processes, Bernhard M, Brinckman FE,Sadler PJ (eds) Dahlem Konferenzen 1986. Springer, BerlinHeidelberg New York, pp 71-83Milner NJ (1982) The accumulation of zinc by O-group plaice,Pleuronec tesp la tessa (L.), from high concentrations in sea waterand food. J F ish Biol 21 : 325-336M611er W (1978) Untersuchungen zum Bleigehalt von Siigwas-serschnecken im Oberrheingebiet (Mollusca: Gastropoda).Arch Hydro biol 83 (3):405 418Moriart y F (1984) Persistent contaminants, compartmental modelsand concentration a long food-chains. Ecological Bull 36:35-45Mfiller G (1983) Fl/isse - vom Menschen verg iftet. Bild dWissensch 5:95-100M/iller G, Prosi F (1978) Verteilung von Zink, Kupfer und Cadmi-um in verschiedenen Organen yon P16tzen (Rutilus rutilus L.)aus Neckar und Elsenz. Z Naturforsch 33c: 7-14Murai T, Andrews JW, Smith RG Jr (1981) Effects o f dietarycopper on channel catfish. Aquaculture 22, 353-357Murphy BR, Atchison G J, McInto sh AW, K olar DJ (1978) Cadmi-um and zinc content of fish from an industrially contaminatedlake. J Fish Biol 13:327Nabrzyski M (1975) Mercury, copper, and zinc content in the meattissue of some fresh-water fish. Bromat. Chem Toksykol 8(3):313-319Ney JJ, Van Hassel JH (1983) Sources o f variability in accumula-tion o f heavy metals by fishes in a roadside stream. Arch Envi-ron Contam Toxicol 12:701-706Norstr6 m R J, McKinnon AE, deFreitas ASW (1976) A bioener-getic based model for pollutant accumulation by fish. Simula-tion o f PCB and methylmercury residue levels in Ottawa Riveryellow perch (Perca f lavescens) . J Fish Res Bd Can 33:248-267Paasivirta J, Sfirkk~ J, Surma-Aho K, Humppi T, Kuokkanen T,Martinen M (1983) Food chain enrichment of organochlorinecompounds and mercury in clean and polluted lakes of Finland.Chemosphere 12 (2) : 239-252Paasivirta J, Heinola K, Humppi T, Karjalainen A, KnuutinenJ, M/intykoski K, Paukku R, Piilola T, Surma-Aho K, Tar-hanen J, Welling L, Vihonen H (1985) Polychlorinated Phenols,Guaiacols and Catechols in environment. Chemosphere 14(5):469-491

P/irt P, Lock R AC (1983) Diffusion of calcium, cadmium andmercury in a mucous solution from rainbow trout. Comp Bio-chem Physiol 76C (2):259-263P/irt P, Svanberg O (1981) Uptake of cadmium in perfused rainbo wtrout (Salmo gairdneri) gills. Can J Fish Aquat Sci 38:937-923Patrick FM, Louti t M (1976) Passage of metals in effluents,through bacteria to higher organisms. Wat Res 10:333-335Patrick FM , Loutit MW (1978) Passage of metals to freshwaterfish from their food. Wat Res 12:395-398Patrick WmH, Gambrell RP, Khalid RA (1977) Physicochemicalfactors reguIating solubiIity and bioavailability of toxic heavymetals in contaminated dredged sediment. J Environ Sci HealthA12 (9) :475-492Peakall DB, Lovett RJ (1972) Mercury: Its occurrence and effectsin the ecosystem. Bio Sci 22 (I ):20-25Pentreath RJ (1973) The accumulation and retention of 65-Zn and54-Mn by the plaice, Pleuronectes platessa L. J. exp mar BiolEcol 12:1-8Pentreath RJ (1977) The accumulation of cadmium by the plaice,Pleuronectes platessa L. and the thornback ray, Raja clavataL. J exp m ar Biol Ecol 30 : 223-232Phillips GR, Buhler DR (1978) The relative contributions o f me-thylmercury from food or water to rainbow trout (Salmo gaird-nero in a controlled laboratory environment. Trans Amer FishSoc 107:853-861Phillips GR, Lenhart TE, Gregory RW (1980) Relation betweentrophic position and mercury accumulation among fishes fromthe Tongue River Reservoir, Montana. Environment Res22 : 73-80Piscator M (1986) The dependence of toxic reactions on the chemi-cal species of the elements. In: The importance o f chemical

8/8/2019 Dal Linger

8/8

98"sp eci ati on" in environmental processes, Bernhard M, Brinck-man FE, Sadler PJ (eds) Dahlem Konferenzen 1986. Springer,Berlin Heidelberg New York, pp 59-70Prosi F (1977) Schwermetalle im Wasser, in Sedimenten und inlimnischen Organismen der Elsenz. Thesis, Uni v HeidelbergProsi F (1981) Heavy metals in aquatic organisms. In: Metal pollu-tion in the aquatic environment, F6rstner U, Wittmann GTW(eds) Springer, Berlin Heidelberg New York (2nd ed.),pp 271-323Prosi F (1983) Storage of heavy metals in organs of limnic andterrestric invertebrates and their effects on the cellular level.In: Heavy metals in the Environment, ed. by G. Miiller, vol. I.CEP Consultants, Edinburgh, pp 459-462Prosi F, Back H (1985) Indica tor cells for heavy metal uptakeand distribution in organs from selected invertebrate animals.In: Heavy metals in the environment, ed. Lekkas TD, vol II,CEP Consultants, Edinburgh, pp 242-244Prosi F, Miiller G (1987) Bedeutung der Sedimente als Schwerme-tallfalle: Bioverfiigbarkeit und MobilitS, yon Met allen in Bezugauf den Biotransfer in limnische Organismen. In : Forschungs-berichte der Deutschen Forschungsgemeinschaft (1987). Bioak-kumulation in Nahrungsketten. Verlag Chemic, Weinheim (inpress).Prosi F, Hoene-Schweikert H, Mfiller G (1979) Verteilungsmustervon Schwermetallen in einem lfindlichen Raum. Naturwissen-schaften 66:573Rainbow PS (1985) The biology of heavy metals in the sea. Intern.J. Environm. Studies 25:195-211Ramamoorthy S, Kushner DJ (1985) Heavy metal binding in riverwater. Nat ure 256 : 399-401Renfro WC, Fowler SW, Heyraud M, La Rosa J (1975) Relativeimportance of food and water in long-term zinc-65 accumula-tion by marine biota. J Fish Res Board Can 32:1339-1345Roch M, Nordin RN, Austin A, McKean CJP, Deniseger J, Kath-man RD , McCarter JA, Clark MJ R (1985) The effects of heavymetal contamination on the aquatic biota of Buttle Lake andthe Campbell River drainage (Canada). Arch Environ ContamToxicol 14:347-362Rygg B (1985) Effect of sediment copper on benthic fauna. MarEcol Prog Ser 25 : 83-89Sfirkk/i J, Hattula M-L, Paasivirta J, Janatuinen J (1978) Mercuryand chlorinated hydrocarbons in the food chain of Lake Pfii-j/inne, Finland. Holarctic ecol 1 : 326-332Sakata M (1985) Diagenetic remobilization of manganese, iron,copper and lead in anoxic sediment of a freshwater pond. WatRes 19 (8): 1033-1038Saward D, Stirling A, Topping G (1975) Experimental studies onthe effects of copper on a marine foo d chain. Mar Biol29:351-361Segner H (1987) Response of fed and starved roach, Rutilus rutilus,to sublethal copper contamination. J Fish Biol (in press)Segner H, Back H (1985) Importance of contaminated food forthe uptake of heavy metals in the rainbow trout, Salmo gaird-neri. Naturwissensch 72:379-380Simkiss K, Mason A Z (1983) Metal ions: Metabolic and toxiceffects. In: The Mollusca, Ho chachk a PW (ed), vol. II. Aca-demic press, New York, pp 102-164Skidmore JF (1970) Respiration and osmoregulation in rainbowtrout with gills damaged by zinc sulphate. J exp bio152:484M94Somero GN, Chow TJ, Yencey PH, Snyder CB (1977) Lead accu-mulation rates in tissues o f the estuarine teleost fish Gillichthysmirabilis: salinity and temperature effects. Arch En vironm Con-tam Toxicol 6:337-348Spehar RL, Anderson RL, Fiandt JT (1978) Toxicity and bioaccu-

mulation of cadmium and lead in aquatic invertebrates. Envi-ron Pollut 15:195-208Stumm W, Keller L (1984) Chemische Prozesse in der Umwelt- Die Bedeutung der Speziierung ffir die chemische Dynamikder Metalle in Gew/issern, B6den und Atmosphfire. In: Metallein der Umwelt. Verteilung, Analytik und biologische Relevanz,Merian E (ed), Verlag Chemic, pp 21-33Sunda W, Guillard RRL (1976) Relationship between cupric ionactivity and the toxicity of copper to phytoplankton. J marRes 34:511-529

Sunda WG, Engel DW, Thuotte RW (1978) Effects of chemicalspeciation on toxicity of cadmium to grass shrimp Palaemonetespugio: Importance of free cadmium ion. Envir Sci technol12:40%413Tarifeno-Silva E, Kawasaki LY, Yut DP, Gordon MS, ChapmanDJ (1982) Aquacultural approaches to recycling of dissolvednutrients in secondarily treated domestic wastewaters -I II . Up-take of dissolved heavy metals by artificial food chains. WatRes 16:59-65Tessier A, Campbell PGC, Auclair JC, Bisson M (1984) Relation-ships between the partition ing of trace metals in sediments andtheir accumula tion in the tissues of the freshwater mollusc Ellip-tio complanata in a mining area. Can J Fish Aquat Sci 41(10): 1463-1472Van der Putte I, Brinkhurst MA, Ko eman JH (1981) Effect ofpH on the acute toxicity of hexavalent chromium to rainbowtrout (Salm o gairdneri). Aqua t Toxicol 1 : 129-142Van Hassel JH, Ney JJ, Garling DL (1980) Heavy metals in astream ecosys tem at sites near highways. Trans Am Fish Soc109:636-643Varanasi U, Markey D (1978) Uptak e and release of lead andcadmium in skin and mucus of coho salmon (Oncorhynchuskisutch). Comp Biochem Physiol 60C:187 191Vighi M (198 I) Lead uptake and release in an experimental trophicchain. Ecotoxicol. Environmen t Saf 5 : 177-193Vinikour WS, Goldstein RM, Anderson RV (1980) Bioconcentra-tion patterns of zinc, copper, cadmium and lead in selectedfish specis from the Fox River, Illinois. Bull Environm ContainToxicol 24:727 734Wachs B (1981) Schwermetal le in Wasser-Organismen - Bioakku-mulation, -magnifikation und -retention. Sicherh Chem u Umw1:113-115Wachs B (1982) Die Bioindikation von Schwermetallen in Flieg-gewS, sern. Mfinchner Beitr z Abwasser-, Fischerei- u Flul3biol34:301-337Westernhagen Hv, Dethlefsen V, Rosenthal H, Ffirstenberg G,Klinckmann J (1978) Fate and effects of cadmium in an experi-menta l marine ecosystem. Helgol wiss Meeresunters31 : 471-484Wiener JG, Giesy JP (1979) Concentrations of Cd, Cu, Mn, Pb,and Zn in fishes in a highly organic software pond. J FishRes Bd Can 36:270Williams DR, Giesy JP Jr (1978) Relative importance of food andwater sources to cadmium uptake by Gambusia affinis (Poecilii-dae). Environ m Res 16:326-332Willis JN, Sunda WG (1984) Relative contributions of food andwater in the accumulation of zinc by two species of marinefish. Mar Biol 80:273 279Yediler A (1978) Anreicherungsverhalten von Zink in Binnenge-wfissern. In: Schadstoffe im Oberflfichenwasser und im Ab-wasser. Miinch Beitr z Abwasser-, Fischerei- u. Flul3biologie30:73-83

Received April 8, 1987