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Oecologia (Berlin) (1987) 73:91-98 Oecologia

9 Springer-Verlag1987

Contaminated food and uptake of heavy metals by fish:


a review and a proposal for further research
R. Dallinger 1, F. Prosi 2, H. Segner 3, and H. Back 3
1 Institut ffir Zoologic (Abteilung Zoophysiologie), TechnikerstraBe 25, A-6020 Innsbruck, Austria
2 Institut ffir Zoologic I (Morphologie/{Jkologie), Im Neuenheimer Fold 230, D-6900 Heidelberg,
Federal Republic of Germany
3 Anatomisches Institut III der UniversitS.t, Im Neuenheimer Fold 307, D-6900 Heidelberg, Federal Republic of Germany

Summary. 1. The uptake of heavy metals via the alimentary centrations of heavy metals in benthic animals and m plants
tract can be an important factor for the metal budget of (McIntosh et al. 1978; Tessier et al. 1984).
fish. 2. Concepts such as biomagnification, bioaccumula- Biomagnification of pollutants is a well known pheno-
tion, biotransference, or concentration factors, convey little naenon, especially with respect to some organic compounds,
information about the real threat originating from heavy like organochlorines or polychlorinated biphenyls (Jarvinen
metals in an aquatic food chain. 3. In polluted aquatic eco- et al. 1977; Paasivirta et al. 1983; Paasivirta et al. 1985).
systems the transfer of metals through food chains can be For heavy metals, however, this assumption is the subject
high enough to bring about harmful concentrations in the of conflicting arguments, and, as stated by Ferard et al.
tissues of fish. This relationship is called the food chain (1983), the term biomagnification has often been misused.
effect. 4. Two kinds of ecological factors influence the food Nevertheless, tissues of many fish species contain elevated
chain effect: firstly, high levels of contamination of the metal concentrations exceeding the nationally or interna-
food, and, secondly, the reduction of species diversity. tionally agreed quality standards for fish meat (F6rstner
When susceptible species are eliminated, metal-tolerant and Mfiller 1974; Nabrzyski 1975; Miiller and Prosi 1978 ;
food organisms may become dominant. Their tolerance Phillips et al. 1980; Czarnezki 1985; Dallinger and Kautzky
may be based either on their ability to accumulate excessive 1985 a).
amounts of metals or to exclude heavy metals from the In this review an attempt is made to evaluate the relative
tissues. These two strategies represent feedback mechanisms contributions of water and food to metal uptake by fish.
which may enhance or weaken the food chain effect. 5. The ecological significance of what is called the food chain
It is concluded that future investigations on transference effect is pointed out. It is concluded that factors influencing
of heavy metals to fish must take into more careful consid- this effect should be subjected to more precise attention.
eration the specific ecological situation of a given environ-
ment.
Bioavailability of metals in water and the pathways of their
Key words: Fish - Food - Heavy metal - Food chain effect up take by fish
In aquatic systems the availability of a metal to organisms
depends on many physico-chemical as well as biological
factors (see F6rstner and Wittmann 1981 ; H~kanson 1984).
Many fish species are among the top consumers of trophic Availability is influenced, for instance, by the chemical spe-
pyramids in aquatic ecosystems. In consequence, they are clarion of ionic recta1 forms, fl~e chemistry of water and
endangered by diet-borne pollutants transferred along the the relative distribution of metals between soluble and parti-
food chain (S/irkk/i et al. 1978; Moriarty 1984). culate fractions. The speciation of a metal in aqueous solu-
The accumulation of heavy metals depends on uptake tions depends on the number and properties of ionic species
via contaminated food and via water, but the relative im- and binding states (Stumm and Keller 1984). Basic prob-
portance of these two avenues for metal uptake often re- lems of metal speciation in seawater have been discussed
mains uncertain. Moreover, the possibility has to be consid- by Millero (1977) and Kester et al. (1986). It has been
ered that in many aquatic ecosystems the bioavailability shown, moreover, that the uptake as well as the toxicity
of heavy metals may have changed during the past years of heavy metals may substantially depend on the chemical
due to increasing efforts in waste water treatment (Jernel6v species involved (Sunda and Guillard 1976; Giesy et al.
and Lann 1971; F6rstner and Mfiller 1974; Wachs 1981; 1977; Sunda et al. 1978; Amiard-Triquet and Saas 1979;
M/iller 1983) or because of the establishment of strict envi- Chakoumakos et al. 1979; Czuba and Mortimer 1980; Van
ronmental standards and laws which regulate emissions der Pntte et al. 1981; Borgmann 1983; Mills 1986; Piscator
(Czarnezki 1985). As a consequence, the greater part of 1986).
heavy metals may now be contained in particulate fractions The chemistry of water itself influences the speciation
because of the decreased concentrations of water-borne of heavy metals in both marine and limnic environments.
ionic compounds. This situation may lead to elevated con- Factors such as hydrogen ion activity (Hgtkanson 1980; Ba-
cini and Suter 1979), hardness (Kinkade and Erman 1975;
Offprint requests to. R. Dallinger Bell 1976; McCarty et al. 1978; Calamari et al. 1980), and
92

salinity (Somero et al. 1977), are reported to be crucial in Table 1. Estimated or quantified (in brackets) relative contributions
this respect. Furthermore, the presence of organic com- of food and water to the accumulation of heavy metals in fresh
pounds and suspended particles may change the activity water fish species. Heavy metals, fish species, relative contributions
of free metal ions (Brown et al. 1974; Ramamoorthy and of food and water, and references are specified. Explanation of
Kushner 1975; Gfichter and Davis 1978; Hirose and Sugi- signs: + +... dominance of one pathway over the other. +...
a positive contribution to metal uptake has been observed
mura 1985; Bernhard and George 1986). Binding to, and
releasing from sediment (Gardiner 1974; Patrick et al. 1977; Heavy metal Fish species Contribution to Reference
Sakata 1985) also affects the availability of metals to aquat- metal uptake from
ic life (Francis et al. 1984; Tessier et al. 1984; Prosi and
Miiller 1987), as do biological or chemical transformations, Food Water
such as the methylation of mercury (Jensen and Jernel6v
1969). Cd Gambusia affinis + ++ a
Among the biological factors affecting metal availabili- Salmo gairdneri + + (?) b
ty, species specific differences like feeding behaviour (Phil- Co-60 Cyprinus carpio ++ + c
lips et al. 1980; Van Hassel et al. 1980; Bernhard and An- Cu Salmo gairdneri ++ + (?) b
Methyl-
dreae 1984; Willis and Sunda 1984; Czarnezki 1985; Loring Salmo gairdneri +§ + d
Hg
and Prosi 1986) and habitat preferences (Delisle et al. 1975; Esox lucius + + (60%?) +
Ney and Van Hassel 1983) play a dominant role. These Perca flavescens + + (60%?) +
basic features are modified by physiological factors, such Pb Salmo gairdneri - ++
as accumulation rates and the binding capacity in an animal Salmo gairdneri + + (?) b
(Pentreath 1977; Jeng and Sun 1981), as well as by ecologi- Poecilia
cal influences like temperature (Somero et al. 1977; Edgren reticulata ++ +
and Notter 1980; Prosi and Mfiller 1987) and feeding habits Zn Salmo gairdneri ++ + (?) b
Rutilus rutilus ++ + (?) i
(Manthey et al. 1979; Mathers and Johansen 1985).
As a consequence, the pathways of metal flux into Williams and Giesy 1978; b Dallinger and Kautzky t985;
aquatic organisms depend on specific features of water Amiard and Amiard-Triquet 1979; d Phillips and Buhler 1978;
chemistry, sediments, and on the biological characteristics Jernel6v and Lann 1971; f Norstr6m et al. 1976; g Hodson et al.
of the organisms. As far as fish are concerned, there are 1978; h Vighi 1981 ; i Yediler 1978
three 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 metals isms of various fish species (Mathis and Cummings 1973;
through the skin. It can be assumed, however, that the Hardisty et al. 1974; Prosi 1977; Anderson et al. 1978; Spe-
body surface of fish is more or less impervious to harmful har et al. 1978; Heyraud and Cherry 1979; Prosiet al. 1979;
substances in the surrounding water. There are some indica- Van Hassel et al. 1980). Moreover, metal-containing food
tions that mucus secretion may prevent heavy metals from represents a much more highly contaminated source than
entering the body of fish (Varanasi and Markey 1978; Lock water, in which the concentrations, even from highly pol-
and Van Overbeeke 1981 ; Eddy and Fraser 1982; Pfirt and luted sites in the field, are lower. Food may therefore be
Lock 1983). an important source of metal contamination in fish. Al-
The assumption that the skin does not play a dominant though most of the work supporting this view is based on
role in the uptake of heavy metals is not true for the gills: laboratory experiments (Hoss 1964; Saward et al. 1975; Pa-
They are not only the main organs of gas exchange, but, trick and Loutit 1976; Aoyama et al. 1978; Jacobs 1978;
as a highly specialized and exposed part of the body surface, Patrick and Loutit 1978; Amiard-Triquet 1979; Amiard
also represent an important site of uptake of essential and and Amiard-Triquet 1979; Hamdy and Prabhu 1979; Jeng
non-essential metal ions from the water (Chartier 1974; and Sun 1981; Vighi 1981; Murai et al. 1981; Knox et al.
Fenwick and So 1974). For instance, after exposure of fish 1982; Milner 1982; Tarifeno-Silva et al. 1982; Ferard et al.
to soluble zinc or cadmium these metals are found in their 1983; Segner and Back 1985), in a few instances the prob-
gills (Hughes and Flos 1978; Westernhagen et al. 1978). lem has been studied in the field (Dallinger and Kautzky
It has been shown by P/irt and Svanberg (1981) that cadmi- 1985 b). It thus appears that gills and gut are both important
um is taken up by perfused gills of rainbow trout, a signifi- pathways for metal uptake in fish (Kumada et al. 1973;
cant uptake occurring immediately after exposure (Ander- Bernhard and Andreae 1984; Willis and Sunda 1984): Solu-
son and Spear 1980; Collvin 1984; Segner 1987). From ble metal fractions may accumulate preferentially via the
the gills, the absorbed metals are distributed throughout gills, particulate metal fractions via the alimentary tract.
the whole body and accumulate in specific organs. Heavy
metals have also been reported to induce harmful changes
The relative importance of food as a source of heavy metals
in gill morphology (Haider 1964; Baker 1969; Skidmore
1970; Van der Putte et al. 1981; Karlsson-Norrgren et al. In only few studies has an attempt been made to quantify
1985). It thus seems that passage through the gills is an or at least estimate the relative contributions of water and
important pathway for the soluble fractions of heavy metals food to metal uptake by fish. Tables 1 and 2 summarize
into fish. some results of such studies for fresh water (Table 1) and
Uptake of particulate metal fractions by fish occurs, marine fish species (Table 2). Most of the data are derived
if at all, from contaminated suspended matter, sediments, from laboratory experiments, in some cases employing ra-
and organisms serving as food sources, the only feasible dioactive nuclides. In situations in which fish are allowed
route being the alimentary tract. In many aquatic systems to take up heavy metals simultaneously from both water
pollution has led to metal contamination of the food organ- and food the latter pathway generally dominates. This is
93

Table 2. Estimated or quantified (in brackets) relative contributions have been reported for lead (compare H o d s o n et al. 1978;
of food and water to the accumulation of heavy metals in marine Vighi 1981), but the reality of the food pathway c a n n o t
fish species. Heavy metals, fish species, relative contributions of be denied. It remains to be seen to what extent laboratory
food and water, and references are specified. Explanation of signs : findings reflect the actual situations in the field. In laborato-
+ + ... dominance of one pathway over the other. + ... a positive ry experiments the food offered to the fish is, as a rule,
contribution to metal uptake has been observed
uniformly c o n t a m i n a t e d with heavy metals; this is certainly
Heavy metal Fish species Contribution to Reference not true for most polluted habitats in nature, where fish
metal uptake from are able to choose between different kinds o f food. Thus
in the field food may be a less i m p o r t a n t source of heavy
Food Water metals than in the laboratory, but its role should not be
underestimated (Dallinger and K a u t z k y 1985 b).
Cd-115 Pleuronectes The uptake of heavy metals from food depends on var-
platessa + + + a ious influences. Some reports indicate that a significant ab-
Raja clavat" + + + " sorption of a metal by fish takes place only, if the metal
Mn-54 Pleuronectes content in the food exceeds a m i n i m u m threshold level (Ja-
platessa + + + b
cobs 1978; Murai et al. 1981). Moreover, feeding frequency
Zn-65 Pleuronectes
platessa + + + b and c o n s u m t p i o n rates (Aoyama et al. 1978; Mathers and
Paralychthys sp. + + (65%) + ~ Johansen 1985), diet quality (Renfro et al. 1975), and inter-
Zn Pleuronectes actions with water-borne metals may modify food-related
platessa + + + metal accumulation in fish.
(10%) d A n i m p o r t a n t question is whether the extent of metal
Gambusia uptake from water or food is reflected in elevated concen-
affinis + + (78%) + trations of different organs. F o r instance, after c o n t a m i n a -
Leiostomus
tion with copper or c a d m i u m high metal contents are found
xanthurus + + (82%) + e
Gobius sp. + + (60%) + e in liver and kidney (Mfiller and Prosi 1978; Edgren and
Notter 1980; Wachs 1982; Dallinger and K a u t z k y 1985b).
a Pentreath 1977; b Pentreath 1973; c Hoss 1964; d Milner 1982; Since these organs are targets for final deposition of various
e Willis and Sunda 1984; f Renfro et al. 1975 heavy metals, the levels in both organs seem to be indepen-
dent of the pathway of uptake. However, it is to be expected
that the contributions of water a n d food to metal uptake
best documented for zinc, the rapid assimilation of which in whole fish are reflected by high concentrations in gills
may be due to its role as an essential trace element. Highly and gut tissue, respectively. Table 3 summarizes some re-
toxic elements like lead a n d c a d m i u m are also assimilated suits comparing the concentrations of different tissues from
fi'om food, c a d m i u m apparently more rapidly in freshwater marine and freshwater fishes contaminated via water and
than in marine habitats. As far as mercury is concerned, via food. In fishes taking up heavy metals from water (Tab-
most observations have involved the methylated metal. le 3 a), the gills generally show higher concentrations than
Lock (1975) observed that in Salmo gairdneri the uptake gut tissues or other organs. O n the other hand, fish accumu-
rate of methylmercury from water was higher than from lating heavy metals from food (Table 3b) show elevated
the food, but the percentage uptake of the metal from the metal levels in the gut compared to gills or other organs.
latter source was 5-10 times higher. Contradictory results Both gills and gut are probably sites of transient metal

Table 3. Comparison 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 concentrations in organs are not quantified, but ranked in decreasing order

Heavy metal Fish species Tissue or organ, ranked by concentration Reference

a accumulation by water
Cd-115 Pleuronectes platessa gill filaments > intestine > liver
Raja clavata gill filaments > liver > intestine
Cd Pleuronectes platessa gills > liver > muscle b
Perca fluviatilis gills > gut ~
Co-60 Cyprinus carpio gills > digestive tract d
Mn-54 Pleuronectes platessa gills > gut e
Zn-65 Pleuronectes platessa gills > kidney > liver > gut e
b accumulation by food
Cd Salmo gairdneri intestine > liver r
Co-60 Cyprinus carpio digestive tract > gills d
Cu Salmo gairdneri liver > intestine r
Hg Cichlasoma facetum gut > liver > muscle > head g
Zn Cyprinus carpio digestive tract > kidney > hepatopancreas > spleen > skin and muscle h
Salmo gairdneri gut tissue > gills i

" Pentreath 1977; b Westernhagen et al. 1978; c Edgren and Notter 1980; a Amiard and Amiard-Triquet 1979; e Pentreath 1973;
f Segner and Back 1985; g Hamdy and Prabhu 1979; h Jeng and Sun 1981; i Dallinger and Kautzky 1985b
94

Table 4. Explanation of formal relationships referring to the uptake of water. Similarly, biotransferencefactors express the con-
of heavy metals by fish. Concepts, definitions, and formulas are centration of a metal in an organism in relation to the
reported next lower trophic level. Several problems are inherent to
these concepts. For instance, the values of bioconcentration
Concept Definition Formula
and biotransference factors change according to the envi-
ronmental medium or food type chosen as reference. This
Biomagnification Metal levels increase
progressively along the trophic can be a problem wherever the primary source of metals
pyramid and their pathways through food chains are not exactly
known. Bioconcentration and biotransference factors ex-
Biotransference Transfer of heavy metals press, in these cases, fictive magnitudes. They are, more-
through successive links
of a food chain over, inappropriate variables for considering and estimating
C~ harmful levels of a given metal within the tissues of a fish.
Biotransference factor Concentration of a metal in TI - It has been found that both bioconcentration and bio-
an organism in relation to transference factors can (but need not) increase along a
the next lower trophic link
given food chain up to the level of the organisms on which
of a food chain.
the fish species feed (Heyraud and Cherry 1979; Bernhard
Bioaccumulation Heavy metals in biota are and Andreae 1984; Dallinger and Kautzky 1985b; Dall-
concentrated in relation to inger 1986). On the trophic level of fish, however, these
abiotic environmental levels
C,c factors are usually reported to decrease again (Enk and
Concentration factor Metal concentration within Cj- Mathis 1977; Amiard-Triquet 1979; Amiard-Triquet and
atrophic component in Ce
Saas 1979; Gfichter and Geiger 1979; Mathis et al. 1979;
relation to abiotic Vighi 1981 ; Tarefeno-Silva et al. 1982; Ferard et al. 1983 ;
environmental levels Bernhard and Andreae 1984). One reason for this is that
heavy metals are more available to organism of lower- than
Explanation of symbols : TI transference factor; C~ metal concen-
tration in atrophic level x; Cx_l metal concentration in the next to those of higher trophic levels. Moreover, fish seem to
lower trophic level x-1 ; CI concentration factor; Ctc metal concen- be able to reject large amounts of the heavy metals ingested
tration in a trophic component; Ce metal concentration of abiotic (Hamdy and Prabhu 1979; Tarifeno-Silva et al. 1982). As
environment mentioned above, this may be true to a greater extent for
non-essential and more toxic elements than for essential
ones. In addition, the comparison of concentration factors
accumulation, their concentrations depending, among other along a food chain may give an inaccurate description of
factors, on the transfer rates at which absorbed metals are the actual metal transfer, since fish concentrate heavy met-
carried to the final target sites in fish. als in certain organs which make only a small contribution
to the total body weight. For a real estimate for the metal
input rate from food such factors as the total amount of
The role of aquatic food chains in metal toxicity
food consumed and the faecal loss of heavy metals have
and accumulation in fish
to be known (Milner 1982).
In order to describe the transfer of heavy metals through The findings that bioconcentration and biotransference
aquatic food chains terms like ~ biomagnification", ~ bioac- factors decrease at the level of the fish should not obscure
cumulation", or "concentration factors", have been intro- the fact, however, that transfer of heavy metals through
duced. Unfortunately, the terms have often been misused food chains remains an important issue in metal assimila-
(Ferard et al. 1983) or carelessely adopted. tion by fish. Most heavy metals are effective at very low
In Table 4 the concepts behind the terms are summa- concentrations, so even low assimilation rates (reflected by
rized and defined (Vinikour et al. 1980; Vighi 1981 ; Wachs small transfer factors) are sufficient to attain biologically
1981 ; Ferard et al. 1983; Dallinger 1986). significant or harmful concentrations in tissues (Jackim
Biomagn~'cation means that metals are progressively et al. 1970; Murai et al. 1981 ; Segner and Back 1985).
concentrated within a given food chain, metal levels increas-
ing with the order of the trophic level. Whether biomagnifi-
Ecological constraints and the food chain effect." possible
cation of heavy metals occurs in fish is a controversial ques-
connections and feedback mechanisms
tion. The hypothesis is supported by some authors (Gold-
water 1971 ; Peakall and Lovett 1972), but rejected by most The concepts of "biomagnification" and "bioconcentra-
others (Leland and McNurney 1974; Giesy and Wiener tion" convey little information regarding the real threat
1977; Wiener and Giesy 1979; Prosiet al. 1979; MeFarlane from heavy metals in an aquatic food chain. Even if bio-
and Franzin 1980; Wachs 1981). Experimental evidence magnification is not observed, or bioconcentration factors
against biomagnification has been presented in several stu- are small, the amount of metal transferred via food can
dies (Knauer and Martin 1972; Amiard-Triquet 1979; be high enough to reach harmful levels in the tissues of
Gfichter and Geiger 1979; Hamdy and Prabhu 1979). aquatic animals, endangering the animals themselves as well
Biotransference is defined as the relative enrichment of as possible predators or consumers (Eisler et al. 1972). We
heavy metals through successive links of food chains. Bioac- shall refer to this relationship as the food chain effect.
cumulation means that heavy metals in organisms are con- An important question concerns the extent to which
centrated in relation to abiotic environmental levels, such the food chain effect in fish may be influenced by ecological
as those of water or sediment. Concentrationfactors indicate conditions. Two possible factors should be considered.
how many times a fish concentrates a metal above a certain The first of these is related to the degree of contamina-
environmental level which is usually (but not always !) that tion of the food supply. It has been shown that heavy metal
95

pollution in aquatic ecosystems is often more markedly re- more careful consideration to the specific ecological situa-
flected by high metal levels in sediments, macrophytes and tion of a given environment. The exclusive measurement
benthic animals than by elevated concentrations in water of metal concentrations in fish, fish food and water, and
(Mathis and Kevern 1975; Enk and Mathis 1977; McIntosh the calculation o f concentration factors can be confusing
et al. 1978; Mathis et al. 1979; Prosi et al. 1979; A b o - R a d y and may lead to conflicting results which are difficult to
1980; Van Hassel et al. 1980; Prosi 1981). This pattern of interpret. The transfer of metals from food to fish can be
distribution may occur with both low- and high-level chron- estimated only when the components of the lower trophic
ic pollution (Dallinger and Kautzky 1985b). Depending on level are analyzed and their contribution to the food o f
their habitat preferences or specialized food requirements fish is evaluated. In order to achieve this end, investigations
fish may be endangered in such situations. It has been on the gut content of fish are necessary. In short, factors
shown, for instance, that bottom-dwelling fish species accu- influencing the food chain effect must be more accurately
mulate heavy metals because of their association with met- considered in order to achieve an understanding of the pro-
al-containing sediments (Delisle et al. 1977; Ney and Van cesses and problems of metal transfer through food chains
Hassel 1983). Ingestion of sediment and of sediment-dwell- into the body of fish.
ing invertebrates may be an important source of metal up-
take by these fishes (Czarnezki 1985; Loring and Prosi Acknowledgements. We thank Prof. Wolfgang Wieser and Joy
1986). It is likely that the food chain effect is enhanced Wieser for reviewing the manuscript. The work was supported by
in those aquatic environments in which metal loaded food, the "Fonds zur F6rderung der wissenschaftlichen Forschung in
such as macrophytes or invertebrates, represent a large ()sterreich", projects Nr. P5962B and S-35/04.
share o f the diet offish (Hardisty et al. 1974; M u r p h y et al.
1978). References
A second kind of influence on the food chain effect
in fish may be due to the reduction of species diversity. Abo-Rady MDK (1980) Makrophytische Wasserpflauzen als
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Leine. Arch Hydrobiol 89 (3):387~404
lead to the elimination of susceptible species (Burmeister
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