The Royal Society

The Effects of Heavy Metals (other than Mercury) on Marine and Estuarine Organisms
Author(s): G. W. Bryan
Source: Proceedings of the Royal Society of London. Series B, Biological Sciences, Vol. 177, No.
1048, A Discussion on Biological Effects of Pollution in the Sea (Apr. 13, 1971), pp. 389-410
Published by: The Royal Society
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Proc. Roy. Soc. Lond. B. 177, 389-410 (1971)
Printed in Great Britain
The effects of heavy metals (other than mercury)

on marine and estuarine organisms
BY G. W. BRYAN
The Laboratory, Citadel Hill, Plymouth
Heavy metals such as copper, zinc and lead are normal constituents of marine and estuarine
environments. When additional quantities are introduced from industrial wastes or sewage
they enter the biogeochemical cycle and, as a result of being potentially toxic, may interfere
with the ecology of a particular environment. In different marine organisms, the behaviour
of heavy metals is described in terms of their absorption, storage, excretion and regulation
when different concentratio-ns are available in the environment. At higher concentrations,
the detrimental effects of heavy metals become apparent and their different toxic effects and
factors affecting them are also described.
1. INTRODUCTION
Heavy metals in trace amounts are normal constituents of marine organisms and
some of them such as zinc, copper and cobalt are absolutely essential for normal
growth and development. In coastal regions, these metals are normally supplied
to the sea in river water or as wind blown material following the weathering of
rocks (see, for example, Schutz & Turekian I965). However, at the present time,
additional quantities of metals are being added to estuaries and coastal regions
from industrial effluents, from sewage and from atmospheric pollution. For example,
high concentrations of zinc may occur in wastes from synthetic fibre production,
from mining, from electroplating or from sewage, and lead in unusually high con-
centrations in sea water off the coast of California has been attributed to atmos-
pheric pollution above the Los Angeles Basin (Brooks, Presley & Kaplan I967).
At sufficiently high concentrations, heavy metals are toxic to living organisms
and so it is important to know by how much their concentrations may be increased
above the normal range in the environment before effects on marine or estuarine
populations can be detected or commercial species become unsuitable as food.
2. THE FATE OF HEAVY METALS IN COASTAL REGIONS

What happens when comparatively high concentrations of heavy metals are
introduced into the sea by rivers or outfalls depenids on several basic factors which
have been discussed in detail by a number of authors (e.g. Krauskopf 1956;
Schutz & Turekian I965; Goldberg I965; Fukai & Huynh-Ngoc I968). In addition
to the effect of dilution in lowering concentrations, at least three other processes
can remove heavy metals from seawater and these are precipitation, adsorption
and absorption by marine organisms.
Precipitation occurs if the concentration of a metal is higher than the solubility
of the least soluble compound that can be formed between the metal and anions
[ 389 ] 25-2

390 G. W. Bryan (Discussion Meeting)
in the water such as carbonate, hydroxyl or chloride. In aerated seawater, the
approximate concentrations of metals which can remain in saturated solution in
the presence of precipitate have been given by Krauskopf (1956) and are shown in
table 1 together with some recent figures for these metals in coastal waters. The
concentrations of heavy metals which can remain in solution are orders of magni-
tude higher than those usually found in the sea and Krauskopf concluded that
normally the sea is considerably undersaturated with heavy metals. In table 1 the
concentrations in saturated solution refer to clean aerated seawater but could, for
example, be increased by the presence of complexing agents or reduced as happens
in anoxic waters when hydrogen sulphide is present. Sulphides of metals such as
zinc, copper, cadmium, lead and silver are very insoluble and so in waters con-
taining hydrogen sulphide these metals are largely precipitated (see, for example,
Krauskopf 1956; Richards I965).
TABLE 1. CONCENTRATIONS OF METALS IN SATURATED SOLUTION IN AERATED SEA-

WATER AT pH 7.8 to 8.2, AND 18 TO 23 0C (FROMKRAUSKOPF 1956) COMPARED
WITH SOME RECENT VALUES FOR COASTAL SEAWATER
concentration
in solution concentration
possible form after several in coastal
metal of precipitate weeks (parts/106) seawater (parts/106)
Zn ZnCO3 1.2-2.5 0.004*
Cu CuCO3 0.4-0.8 0.005*
Pb PbCO3 0.3-0.7 0.00t
Cd Cd(OH)Cl 4-1000 0.00006*
Ni Ni(OH)2 20-450 0.004*
Co Co(OH)3 25-200 0.0001*
CoCO3
Ag AgCl 2.0-2.5 0.00015T
Cr(6) CaCrO4? high 0.0004?
*
Riley & Taylor (I968). t Loveridge et al. (I960).
Soyer (I963). ? Fukai & Vas (I967).
Adsorption of metals from solution occurs at the surfaces of particulate materials

such as clays, phytoplanktonic organisms, hydrated ferric oxide and hydrated
manganese dioxide. Of these last two materials, hydrated ferric oxide is usually
more important in coastal regions because it is generally more abundant and
soluble iron is more readily precipitated than manganese. Experiments by Kraus-
kopf (1956) and Fukai & Huynh-Ngoc (I968) have shown how all heavy metals
are not equally readily adsorbed. Zinc, copper and lead are probably readily
adsorbed by both hydrated ferric oxide and hydrated manganese dioxide but
cobalt and nickel show a stronger affinity for hydrated manganese dioxide and
silver is not readily adsorbed by either material. Nor is chromium as chromate
unless it is first reduced to the trivalent form which is readily co-precipitated in
the presence of iron (Fukai & Huynh-Ngoc I968).

Effects of heavy metals 391
Because different heavy metals are not equally readily precipitated or adsorbed,
some metals will be deposited in sediments extending different distances from the
source of supply, whereas other metals in solution will be dispersed farther afield.
This type of behaviour is shown quite clearly when mixtures of radioactive wastes
are discharged into the sea and is very important in determining the distribution
of these elements to marine organisms (see, for example, Preston & Jefferies I969).
Heavy metals are also removed from seawater when they are accumulated by
marine organisms. Concentration factors for different metals vary considerably
from species to species but factors of hundreds or thousands are commonly found
and occasionally a factor of a million may be approached (see, for example, Fukai
& Broquet I965; Bryan, Preston & Templeton I966; Fukai I968). However, many
organisms also live and feed in sediments and undoubtedly absorb metals from
them. So it should not be assumed that only metals derived from solution in sea-
water, either directly or through food chains, are available for marine organisms.
3. BEHAVIOUR OF HEAVY METALS IN MARINE ORGANISMS

In the following sections the absorption, excretion, storage and regulation of
heavy metals will be discussed.
(a) Absorptionfrom solution

Absorption from solution in seawater may occur across the general body surface
of an organism or through special areas such as gills and if an animal such as a
teleost fish drinks seawater then absorption across the walls of the gut may also
occur. As an example of how a metal can be absorbed from solution in seawater by
an animal, the absorption of zinc by the lobster Homarus vulgaris will be used.
The blood flowing through the gills of a lobster contains about 7 parts/106 of zinc
which is 103to 104times the concentration in seawater. However, this does not mean
that in order to maintain the concentration gradient across the gills zinc must be
absorbed by an active tr,ansport process. In the blood, zinc is so tightly bound to
proteins such as haemocyanin that the concentration gradient for unbound zinc
favours its diffusion fromrthe water through the gills into the blood. The actual
process is not quite as simple as this because, before it diffuses through the gill
epithelium probably attached to proteins, the zinc is first adsorbed onto the cuticle
covering the gills. Rates of absorption of zinc in whole lobsters and in the isolated
gills at different seawater concentrations of zinc are shown in figure 1. Probably
because adsorption is involved, the rate of absorption is not proportional to the
seawater concentration of zinc. This is probably of advantage to the lobster
because, compared with the slope of the broken line in figure 1 which represents
proportional uptake, relatively more zinc is absorbed from low concentrations but
relatively less from high concentrations.
This type of absorption process is not necessarily universal for all metals in all
organisms but it may be fairly widespread. Absorption of a similar type has been

described for a much simpler system, the egg of the coho salmon, by Wedemeyer
(I968), who concluded that zinc uptake from freshwater depends initially on
physicochemical sorption onto the chorion followed by passive diffusion into the
yolk and embryo.
/ ~~~0
102
bio'
0
.;~~~~~~~- ,'
0~~~~~
/ /
0~ ~~~
1-
10-3 lo- 2 1002
zinc in seawater (parts/106)

FIGOURE 1. Rates of absorption of zinc in the lobster, Hornarus vuglaris, at about 13 ?C.
O, Rates for 500 g whole lobsters acclimatized to different seawater concentrations
of zinc; o, zinc absorbed per gramnof isolated gills during first day of absorption from
different seawater concentrations of zinc; ---, slope of line if absorption proportional to
seawater concentration of zinc.
Absorptionby individual tissues also appearsto involve sorption at sites on and

within the cells. In the liver of the pufferfish Tetraodonhispidus the accumulation
of zinc against an apparent concentration gradient was found to be a passive
process not directly coupled to metabolic energy (Saltman & Boroughs I96o).
As absorption appears to lbe a passive process, attempts have been made to
relate concentrationfactors for differentmetals in whole organismsor tissues to the
stabilities of complexes formed between the metals and organic ligands. Probably
because there are so many different ligands and because the concentrations of
essential metals such as copper or zinc are sometimes regulated by the organism,
this approach has not been particularly successful. For example, brown seaweeds
such as Lalmiynabria digi?taltacontain alginates in the cell walls and intereellular
spaces which act as ion exchange materials and have a strong affinity for divalent
metals. Haug (I96I) has shown that in alginate extracted from the weed the
affinity for divalent metals decreases in the order
Pb > Cu > Cd > Ba > Sr > Ca > Co > Ni, Zn Mn > Mg.
Resulzs obtained by Haug & Smidsred (I967) have strongly suggested that the
distribution of strontium, calcium and magnesitrHmbetweenLvlminari,at and sea-
water is largely explained by this affinity between divalent metals and alginate.

Although this might also explain the distribution of some of the heavy metals it
does not apply to zinc. Concentration factors of about 2500 for zinc exceed those
for copper and it is thought that other materials such as cell proteins may govern
its distribution (Bryan I969).
x ~~~~~~~0
200 -
100 0
4 0
? 50
20 -
0~~~~
Q I
N -| \
2 /- \
1 l
0 25 50 100 300 500
time/h
FIGURE 2. Absorption of 3 mg of zinc from stomach fluid in 300 g lobsters Homarus vulyaris
(after Bryan i964). Concentrations in: x, stomach fluid; *, blood; o, hepatopancreas;
?, urine.
(b) Absorptionfrom food or ingestedparticles

Absorption from the digestive tract can be an important source of heavy metals
in animals, Results obtained by Hoss (I964) using 65Zn in the flounder, Para-
lychthys, have suggested that food is probably a more important source of zinc
than seawater and work on the oyster, Ostrea edulis, by Preston & Jeifries (I969)
has shown that metals such as zinc and cobalt are probably absorbed from ingested
particles rather than from solution. In the lobster, Homarus vulgaris, metals such
as zinc, cobalt and manganese are rapidly absorbed from the stomach fluid even
if almost toxic concentrations are present and there is no evidence that the animal
can control the rate of absorption if too high a concentration is present (Bryan

I964; Bryan & Ward I965). As an example, the absorption of zinc from the stomach
fluid of the lobster and its appearance in the blood and hepatopancreas is shown in
figure 2.
(c) Excretion
Because some heavy metals are so readily accumulated by marine organisms the
main problem for most organisms is often not one of absorption but one of removal.
If, as in figure 2, a metal is absorbed in excess by one of the higher animals, there
are potentially three ways of removing it from the body.
The first way is by losing the metal back across the body surface or gills and
excretion of zinc across the gills appears to occur in the shore crab, Carcinus
maenas (Bryan I966), and in the rainbow trout, Salmo gairdnerii (Nakatani I966).
The second method is by excreting the metal into the gut. Although in the
lobster Homarus this route is unimportant for the removal of zinc, it is the principal
route in the freshwater crayfish Austropotamobius pallipes pallipes which is a related
species (Bryan I967). In the cyprid larva of the barnacle, Balanus amphitrite
niveus, excess copper is excreted into the lumen of the gut (Bernard & Lane i96I)
and in Octopus dofteini both copper and zinc are excreted in the rectal fluid (Potts
& Todd I965).
Excretion in the urine is the third way of removing metals from the body and
it can be seen in figure 2 that the concentration of zinc in the urine of the lobster
is related to changes in the concentration of zinc in the blood. Crustaceans are also
able to excrete copper, cobalt, manganese and mercury in the urine (Corner I959;
Bryan & Ward I965; Bryan I968) and among molluscs, Octopus dofleini, is able
to excrete copper and zinc in its urine (Potts & Todd I965). Very little information
is available about fish, but in rainbow trout the excretion of zinc in the urine appears
to be relatively unimportant (Nakatani I966).
(d) Storage
A fourth method of removing metals is by storage, usually for a temporary
period, in a particular tissue. In the lobster, for example, excess zinc in the blood
can partially be removed by absorption in the hepatopancreas (see figure 2) and
can then be lost gradually either in the urine or across the body surface. Other metals
are also stored in crustaceans and in the shrimp, Crangon vulgaris, excess copper
appears to be stored as granules in the cells of the hepatopancreas (Djangmah
1970). Several different sites for storing metals have been recognized in bivalve
molluscs. In Scrobicularia plana zinc, lead and cadmium are stored in the hepato-
pancreas but in the scallop, Chlamys opercularis, storage occurs in the renal organs.
These organs account for about 0.5 0 of the mass of the scallop without its shell
but, even under normal conditions, they may contain more than 50 % of the body
burden of some metals (see table 2). Extremely high concentrations of zinc and
manganese occur in these organs and they appear to be stored and probably
excreted as granules. In oysters it has long been known that excess copper is stored
as granules in wandering leucocytes (Boyce & Herdman I898) and it seems likely

that some other metals may be stored in the same way and then gradually elimin-
ated (Galtstoff I964).
TABLE 2. METALS IN THE WHOLE BODY AND RENAL ORGANS OF THE SCALLOP
CHLAMYS OPERCULARIS FROM THE ENGLISH CHANNEL
Mean values for animals collected at six intervals during one year.
concentration proportion
in whole concentration of total
body minus in renal metal in
shell (parts/106 organs (parts/106 renal organs
metal wet mass) wet mass) (%)
Zn 71 8582 60
Mn 21.9 3547 81
Fe 16.4 66.4 2
Cu 2.3 240 52
Pb 1.7 148 43
Ni 0.22 15.8 39
Co 0.05 3.4 34
(e) Regulation
By combining the processes of absorption, excretion and storage, the higher
animals, at least, should potentially be capable of regulating the concentrationsof
heavy metals in the body despite changes in their availability in the environment.
How well organisms are able to do this can be checked by exposing them to
different concentrations of a metal and then analysing the tissues.
(i) Zinc in Carcinusmaenas

Concentrations of zinc in the tissues and body fluids of the shore crab after
32 days exposure to different seawater concentrations of zinc are shown in
figure 3. Although there is a 500-fold change in the zinc concentrationof the water,
the concentration in the blood is only doubled. The highest concentrations of
zinc are reached in the hepatopancreasand gills and this is related to the fact that
excess zinc can be stored in the hepatopancreasor excreted across the gills (Bryan
I966). In addition, some zinc is excreted in the urine and consequently the con-
centration of the blood is not changed too radically. As a result, tissues such as
muscles and gonad are able to maintain remarkably constant concentrations.
Although a considerableamount of zinc is adsorbed by the shell as the seawater
concentration increases, the concentration in the whole animal changes by only a
factor of four for a 500-fold change in the external concentration and regulation
is therefore quite good.
(ii) Lead in Crassostreavirginica

In contrast to the crab, results obtained by Pringle, Hissong, Katz & Mulawka
(I968) for the amount of lead absorbed by the eastern oyster after 49 days show
that concentrations in the tissues are almost exactly proportional to different

concentrations in the water (see figure 4). At first sight this appears to show that
oysters are completely unable to regulate lead. However, although they may not
regulate efficiently in the sense of removing excess lead very rapidly from the body,
they may be able to control lead as they do copper by storage in the blood cells
or tissues and can certainly lose it when the seawater concentration is reduced.
However, it does mean that the concentration of lead in the oyster will come to
reflect the average concentration of available lead in the environment.
80
(a)
40*
0~~~~~~
I3 I 111111i t 1?Igt a11,h
aD240 -
(b) A
120 /
0. s*l 1t I @* l l l ^ l,,
lo-, 10-2 iff-I 100
zinc inr seawater (parts/106)
ZFiGuRE 3. Zinc in the tissues of the crab, Carcinus rnaenas, after exposure to different con-
centrations in seawater for 32 days at about 13 'C. Points are mean values for at least
2 crabs. (a) Concentrations in: o, blood; (i), excretory organs; *, muscle; *, male
gonad ; G, urine. (b) Concentrations in : *, shell ; x, gills ; o, hepatopancreas ;
whole crab.-
(iii) Laminaria digitata and Fucus vresicullosus

A similar type of relationship to that for oysters is found for zinc, copper and
lead in brown seaweeds and figure 5 shows how the concentration of zinc in
Lamitnaria digitata reflects the concentration in the water after 42 days exposure.

400
0
+~200-
0 0.1 0.2
lead in seawater (part/106)
Frwuim 4. Lead in the tissues of the oyster Crassostrea virgini$caafter exposure to different
concentrations in seawat;er for 49 days (after Pringle et al. I968). Concentrations in:
*, muscle; x, gills; (@,gonad; o, hepatopancreas.
0~~~~~~
102
10 0.1 0.2 J
bt)
li
i-3 1072 lo 1 100

zine in seawater (part/106)
FIGURE5. Zinc in Lamtnartia dithtata after exposure to different concentrations in seawater
for 42 days (after Bryan I969). ---, Slope if concentration in weed were proportional to
that in seawater.

Especially in organisms which seem to be poorly equipped for excreting metals,
the time of exposure is a very important factor, because uptake tends to become
a cumulative process which may be harmful when critical internal concentrations
are reached (see ? 4cii). Even under comparatively normal conditions, time or age
can be an important factor determining the concentrations of metals in an organism.
In the brown seaweed FucU8 ve8icu108u8 concentrations of metals increase
considerably with the distance of the tissue from the growing point (see figure 6).
This change is probably due to the slow accumulation of these metals, to the syn-
thesis of more binding sites as the weed grows older (hence the increase in dry
mass) and probably to some contamination of older surfaces of the plant by fine
particles.
200
stipe oldthallus new thallus
,
, II
I I
I I I
100 -1 --I I4
I601 -
0 200 400 600~~~~~~6
distance from holdfast/mrn

FIGURE,6. Distribution of metals along the holdfast, stipe and thallus of F7ucus vesiculom?z
from the Tamar Estuary. Concentrations of: *, zinc; o, copper; x, lead; o, per-
centage dry mass.
(iv) Nereis diversicolor

So far, regulation has been considered mainly in relation to cbanges in the
concentrationsof metals dissolved in seawater. Sediments sometimes contain high
concentrationsof heavy metals and yet animals such as worms and molluscs live

in sediments and feed from them without being harmed. The results in table 3
compare the concentrations of metals in two different estuarine sediments and
the concentrations of the same metals in the polychaete worm Nerei8 diver8icolor.
Before analysis these worms were cleaned and allowed to empty the gut. Differ-
ences between the concentrations in the worms are considerably less than differ-
ences between the sediments. Until more is known about the interstitial water and
how tightly the metals are fixed in the sediments it is not possible to be certain,
but the results suggest that Nereis is able to regulate concentrations of some metals
in its body against changes in the sediments. What is not yet known is how
high sediment concentrations must be in order to produce toxic effects.
TABLE 3. METALS IN NEREIS DIVERSICOLOR FROMTWO ESTUARINE

SEDIMENTS
Sediments and worms were digested in nitric acid and after dilution
the supernatantsolution was analysed.
concentrationin sediment
A mean concentrationin ten Nereis
Plym Estuary TamarEstuary , --
(parts/106 dry (parts/106 dry Plym Estuary Tamar Estuary
metal matss) mass) (wet) (wet)
Zn 288 528 34.0 36.0
Cu 49 407 9.0 22.0
Pb 56 230 0.7 1.1
Mn 55 333 1.4 2.2
Fe 5693 37391 86.0 118.0
Although very few species have been studied, it seems fairly clear that some
organisms or individual tissues will reflect the concentrations of heavy metals in
the environment and may be suitable as indicator species, whereas others will
not. Even in animals whexrethe concentration of a metal is regulated, some tissues
such as the gills or hepatopancreas may accumulate high concentrations and this
raises the question of the detrimental effects of heavy metals either on the organ-
isms themselves or on their use as food.
4. DETRIMENTAL EFFECTS OF HEAVY METALS

(a) Lethal effects
Most information on the lethal effects of metals on marine organisms deals with
copper or mercury in fouling organisms (see, for example, Barnes & Stanbury I948;
Corner & Sparrow I956; Wisely & Blick I967), although some information is
available on other metals such as chromium (Raymont & Shields I964) and
cadmium (Shuster & Pringle I969).
The concentration of a, heavy metal which will kill an aquatic organism is very
dependent both on the metal and on the organism. Generally speaking, mercury,
silver and copper are the most toxic metals, followed by cadmium, zinc and lead
and then by chromium, niickel and cobalt. This order of toxicity is not rigid and is

different in different species. Sometimes one metal may be more toxic than an-
other at low concentrations and less toxic at high concentrations.
The susceptibility of different species to heavy metals can vary enormously and,
as an example, the toxicity of copper (as citrate) to the nauplius larva of the
barnacle Elminius modestus and to the copepod Acartia clausi is compared in
figure 7. For Elminius the threshold of toxicity is about 10 parts/106, whereas for
Acartia it is about 0.3 part/106. A threshold value is often found in metal toxicity
experiments and is the concentration at which the curve becomes virtually parallel
to the time axis. However, this value is not simply a function of the particular
metal and the species of organism involved. It can be changed by a whole range of
different factors which influence heavy metal toxicity. These have been studied
principally in freshwater fish and have been fully described by several authors
(e.g. Lloyd & Herbert I962; Skidmore I964; Jackson & Brown I969). There is no
reason to suppose, however, that most of these effects will not apply equally to
marine organisms.
40
20r
20
4-
10
6 0
4\
0~~~~~~
0
2-
10-1 100 101 102

copper in seawater (parts/i106)
FIGURE 7. Toxicity of copper (as citrate) to o, Acartia clausi and; ., larvae of Elminius
modestus (after Corner & Sparrow I956).
(b) Factors influencing toxicity

In table 4 factors which may change the toxicity of a heavy metal to an aquatic
organism are summarized. Much of the information comes from experiments with
freshwater fish and many of the references given for specific factors may cover
other factors equally well. No attempt will be made to discuss all the points in
table 4, but some of the more important aspects will be considered.
The form of the metal in the water is particularly important. Whether or not
a complexed or chelated form of a metal is less toxic than the ionic form seems to

depend on its stability and how easily it can dissociate and give up the metal to
the absorption system of the organism. This reasoning has been used by Herbert &
Vandyke (I964) to explain why the copper-ammonium complex appears to have a
toxicity to rainbow trout which is similar to that for copper ions, whereas the more
stable copper-cyanide complex is less toxic to fish than copper ions (Doudoroff
I956). On the other hand, at concentrations where ions would be precipitated,
metal complexes can remain in solution and in effect become more toxic (hence the
use of copper citrate in figure 7). Other forms of a metal may be more toxic than
the inorganic ions and organo-mercury compounds, which are lipid soluble and
penetrate rapidly into aquatic organisms, are much more toxic than mercuric
chloride (Corner & Sparrow I957). It might be expected that precipitated metals
or those adsorbed onto particles would have a low toxicity, except perhaps in
filter feeders, but Lloyd (I960) and Herbert & Wakeford (I964) found that pre-
cipitated zinc exerted a toxic action on fish. Others, including Sprague (I964a),
have explained their results on the basis that precipitated metals exert very little
toxicity and so there is a strong case for studying this question of the toxicity of
particulate materials in more detail.
In the absence of much evidence to the contrary, it seems reasonable to suppose
that most of the factors affecting toxicity owe their influence to changing the rates
at which metals are absorbed and this could easily be checked if radioisotopes
were used more often in toxicity experiments. For example, using isotopic mercury,
Corner & Rigler (I958) showed that the difference between the resistance of the
larvae of Artemia saluna and Elminius modestus to mercury depends on differences
between the permeabilities of the two organisms, and hence on the rates of uptake,
rather than on differences between the resistance of the tissues.
The antagonistic or synergistic influence of one metal on another may be
explained in the same way. For example, the rate at which zinc is absorbed is
reduced by calcium in the freshwater crayfish and by manganese in the brown
seaweed Laminaria digitata (Bryan I967, I969). Alternatively, one metal may
increase the rate of absorption of another by increasing the permeability of the
body surface and this has been proposed as a possible explanation of the synergistic
behaviour of copper and mercury in small crustaceans by Corner & Sparrow (I956).
Changes in salinity with the tidal cycle would be expected to be a particularly
important factor in relation to metal toxicity in estuaries. However, experiments
with different organisms have given completely different answers. In the amphipod
]arinogammarus marinus Hunter (I949) found that the toxicity of copper in-
creased with decreasing salinity, but Pyefinch & Mott (I948) found that in the
cyprid larva of the barnacle Balanus balanoides the toxicity of copper was lower in
diluted seawater. It was noted that this last result might be explained by the lack
of activity shown by larvae in dilute seawater, because active animals are generally
more susceptible to poisons (see table 4). In contrast to these results, Herbert &
Wakeford (I964) found that smolts of the salmon, Salmo salar, were more resistant
to zinc in 30 to 40 % seawater than in higher or lower concentrations. The reason

w O) Q)Ot a
9 'TI .,.q
I- P)~ ~~P
Q NN 0
c\
Eri
E4~
?1 bO '0o+
E- !g , Pg R 5C a9 ; 4-
H ;, 2o
-4Dc
H~~~~~~~~~~~~~~4C -
4"-
0~~~~~4
~ O
3H, ~ ~ ~ ~B ~ a~ 9 ~g ~c ~ ~
~~~~~~ j
1
i
4 -
$a4 4 I2;c

for this resistance maximum seems to be related in some way to the fact that the
salmon regulates the osmotic concentration of the blood at the equivalent of 30 to
400 seawater. What is not clear is whether the salmon is more resistant in this
concentration of seawater because the stress of having to carry out osmotic or
ionic regulation is minimal or again because zinc is absorbed more slowly through
the gut or gills under this set of conditions.
If the majority of factors listed in table 4 operate by changing the rates at which
heavy metals are absorbed, then they will presumably also influence the rates at
which any sublethal effects become obvious.
(c) Sublethal effects

Exposure to moderate concentrations of heavy metals can produce a variety of
recognizable effects without actually killing an organism and these have been
divided into morphological changes, inhibitory effects and behaviour changes.
(i) Morphologicalchanges
Some effects of metals may be recognized as changes in the shape or colour or
even the taste of edible organisms and the classical example of this is that of
oysters turning green with accumulated copper (see, for example, Boyce & Herd-
man I898). In the oyster Crassostrea virginica this greening has been shown to
occur at a soluble copper concentration of about 0.025 part/106 which is roughly
an order of magnitude higher than the concentration in coastal seawater (Shuster
& Pringle I969).
Histological changes have been found in the tissues of freshwater fish and
crustaceans after exposure to moderate concentrations of metals such as copper,
zinc and lead (see, for example, Crandall & Goodnight I963; Hubschmann I967;
Brown, Mitrovic & Stark I968). Recent work by Baker (I969) using the winter
flounder, Pseudopleuronectes americanu,s, showed that chronic exposure to copper
concentrations of the order of 1 part/106 in seawater produced changes in the ap-
pearance of the gills and a variety of other effects including necrosis of the kidneys
and fatty metamorphosis of the liver. At a concentration of 0.18 part/106 the
principal effects were seen- in the gills and one of the changes involved the replace-
ment of the mucus cells of the gill epithelium by the so-called chloride cells. Baker
speculates that these chloride cells might excrete copper, and this could explain
why, in some fish, acclimatization to sublethal concentrations of a metal can sub-
sequently increase the resistance of the fish to higher concentrations.
For many years heavy metals have been used in experiments on the development
of sea-urchin eggs (see, for example, Rulon I957; Lallier I959; Wilson & Arm-
strong I96I; Timourian I968). Timourian studied the development of the fertilized
eggs of Lytechinus pictu8 and showed that, when embryos were exposed to
0.06 part/106 of zinc in seawater from fertilization until the formation of the pluteas
larva, development was slowed and 250 of the larvae were structurally abnormal.
Even at 0.006 part/106 of zinc, which is a concentration that might be encountered
26 Vol. I77. B.

in coastal water, more abnormal larvae were found than in the control experiments.
It was concluded that the developing larvae accumulate zinc until a critical con-
centration is reached which affects protein synthesis, cell division and cell migration
and thus produces abnormal larvae. Obviously at lower concentrations a later
stage of development can be reached before a critical amount of zinc is accumu-
lated.
(ii) Inhibitory effects

One of the most important and easily measured effects of moderate concentra-
tions of heavy metals is their effect on growth. The essential metals such as zinc
and copper are necessary for proper growth, but the optimum concentrations are
presumably those normally found in the environment and higher concentrations
generally lead to inhibition. This has been found in all organisms from fish and
crustaceans (see, for example, Dilling, Healey & Smith, I926; Hubschmann I966)
to phytoplankton and bacteria (see, for example, Mandelli I969; Jones I967).
Results of an early experiment by Miller (I946) are illustrated in figure 8 and
show how even low concentrations of copper can inhibit growth in the extoproct
polyzoan Bugula neritina which is a fouling organism. More recently, experiments
with the larvae of the sea urchin, Paracentrotus lividus, by Soyer (I963) and Bougis
(I965) have shown that growth is inhibited by 0.01 part/106 of copper, or about
ten times the concentration in the sea, and by only 0.0006 part/106 of silver which
is about four times the concentration in the sea. In the brown seaweed, Laminaria
digitata, growth is inhibited by zinc (Bryan I969) and in figure 9 the results of
similar experiments with lead and copper are shown. The general difference
between the rates of growth of weed in the lead and copper experiments is simply
due to the pieces being from different plants collected at different times of year.
Lead does not appear to affect growth until a concentration of between 0.1 and
0.5 part/106 is used. At 0.5 part/106 inhibition of growth occurs rather suddenly
after the weed appeared to be growing normally and this probably happens when
a critical amount of lead has been absorbed. Growth is also stopped by 0.051
part/106 of copper but is still inhibited at 0.011 part/106 or about ten times the
concentration found in the sea.
In addition to inhibiting growth, heavy metals may have other effects such as
preventing the settlement of sessile organisms such as barnacles (see, for example,
Pyefinch & Mott I948). There is also evidence from freshwater fish that metals can
inhibit feeding (Edwards & Brown I967) and may delay or prevent the approach
of sexual maturity and spawning (Mount i 968). Mount exposed fathead minnows to
hard freshwater containing copper for long periods and found that at 0.095 part/106
half the fish were killed, sexual development was retarded and spawning was pre-
vented. However, the most important observation was that at 0.033 part/106
survival and physical appearance were unaffected but spawning was still prevented.

(iii) Behaviourchanges
Laboratory experiments with young salmon, Salmo salar, have shown that in
soft tapwater containing 0.002 part/106 of copper and 0.003 part/106 of zinc, the
fish are able to detect and avoid additions of only 0.0023 part/106 of copper and
0.053 part/10 of zinc (Sprague I964b). Also, migrating salmon in a river were turned
back by sublethal concentrations of zinc and copper although the avoidance
thresholds were not as low as in the laboratory (Sprague, Elson & Saunders I965).
increase increase
in length/mm in mass (%)
0.8
I'
120 '
/ ,
/ ,
/O~~~~
0/~~~
0.4~~~~~~~~~~~~~~~~~~
(00-~
.40122 ~02 ~ ~ ~ ~ ~ ~ ~~~"
copper in seawater (part/106) time/days

FIGURE 8 FIGURE 9
FiG-uRE 8. Effect of copper on growth in Bugula6 neritina ancestrulae after 5 days (after Miller
I 946) a
FIGURE 9. Effect of different concentrations of lead and copper on growth of pieces of Lamib-
naria digitata. ---, Lead experiment: *, nearly 0 part/106; o, 0.1 part/106; x, 0.5
part/106. -, Copper experiment: *, 0.0012 part/106, o, 0.011 part/106, x, 0.051
part/106.
It is clear from the last three sections that in some instances remarkably low
concentrations of heavy metals in solution can produce detrimental effSects.
Despite the fact that experiments with marine organisms tend to be carried out
with fairly tough species, effects of metals such as copper, silver and zillc have
been recognized at conce-ntrations which are only an order of magnitude higher
26-2

than those found in the sea. Other species, perhaps mainly those from the
sublittoral zone and especially their larvae, may be affected at still lower concentra-
tions. At the present time there is far too little information for any proper assess-
ment to be made. It is not known which species or types of organisms are the most
sensitive to heavy metals. For example, sessile organisms, which are unable to
avoid changes in the environment, may be more tolerant than other organisms.
Susceptibility may depend on the permeability of the organism to different metals
or to its feeding habits or to the efficiency of its regulatory or detoxification system.
Also, the ability of a species to regulate heavy metals may be less efficient in the
larval than in the adult stage and it is not known whether metals such as zinc,
copper and cobalt which are known to be essential metals are better regulated
than those such as lead or mercury which appear to be inessential.
(d) Basic effects

Only the visible effects of heavy metals, for example, in killing an organism or
inhibiting its rate of growth have been considered so far. The basic action of
heavy metals is thought to be due mainly to the inhibition of enzyme systems
except at high concentrations when they act on the surface tissues as protein pre-
cipitants. When rainbow trout are treated with high concentrations of zinc sulphate
the gills are obviously damaged and death is thought to be due to tissue hypoxia
resulting from the prevention of proper oxygen exchange (Skidmore I970). This
may be because the damage increases the diffusion distance from the water to the
blood and need not necessarily be explained in terms of enzyme inhibition. Lethal
effects of metals such as copper in crustaceans have been tentatively ascribed to
the inhibition of respiratory enzymes or of enzymes relating to the excretion of
metals from the gills (see, for example, Corner & Sparrow I956; Kerkut & Munday
I962; Hubschmann i967). The function of many metals in the tissues is to activate
enzymes but this must be done at fairly finite concentrations. If the concentration
is exceeded, then a metal may start to inhibit the enzyme it was previously
activating, or other enzymes, by blocking reactive sites such as sulphydryl groups
which are responsible for catalytic activity. Histological changes in the tissues of
fish or crustaceans following chronic exposure to metals are thought to be mainly
secondary effects resulting from what is virtually starvation produced when the
processes involved in food utilization are inhibited (see, for example, Crandall &
Goodnight I963). Similarly, effects on growth and development have been put
down to the inhibition of enzymes involved in protein synthesis and cell division
(Timourian I968). So that, depending on the metal, its degree of accumulation and
the vulnerability of different enzyme systems many different effects are possible.
5. DiscussioN
Far too little is known, particularly about the ecological effects of heavy metals,
to draw any hasty conclusions. Results from experiments should certainly lead

us to look out for some detrimental effects on the marine ecosystem when soluble
concentrations of metals such as copper, silver or zinc are about ten times the
normal value for sea water. We also know that the concentrations of metals in
some sessile organisms such as brown seaweeds and some molluscs tend to reflect
the concentrations in the water and might, after further study, be used as indicators
of chronic metal pollution. Individual tissues, such as gills or hepatopancreas, of
some organisms might also prove useful as indicators.
Whether or not an organism which is used for food becomes an important path-
way for the metal back to man depends on the metal and on the organism or
tissue which is eaten. For example, when concentrations of metals such as zinc
or copper in seawater are increased, the concentrations in oysters increase appreci-
ably (Shuster & Pringle I969), but in the flesh of crustaceans such as crabs or
lobsters they remain comparatively constant. Thus, potentially hazardous food
organisms or tissues are those which can accumulate and to a large extent tolerate
high concentrations of heavy metals long before they themselves become obviously
affected. Clearly, sessile organisms which are unable to avoid pollution are likely
to be the most troublesome.
Although only a few heavy metals have been studied in detail in a few marine
species, the differences which have been found between different metals and different
organisms have been considerable. In order to be able to make any generalizations
we need to know more about the behaviour of metals in different organisms in
relation to the environment. This does not mean simply in relation to the soluble
concentration in the water because, as was shown earlier, feeding and the ingestion
of inorganic particles may be important sources of metals. Sediments in particular
are likely to be important because of the long-term build up of metals which is
possible in sediments and because they often contain vast numbers of organisms
which may be just as important in the ecosystem as the more obvious species.
I should like to thank Miss J. Butchers for her help in preparing this paper.
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The Effects of Heavy Metals (other than Mercury) on Marine and Estuarine Organisms

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The effects of heavy metals (other than mercury)

2. THE FATE OF HEAVY METALS IN COASTAL REGIONS

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TABLE 1. CONCENTRATIONS OF METALS IN SATURATED SOLUTION IN AERATED SEA-

Adsorption of metals from solution occurs at the surfaces of particulate materials

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3. BEHAVIOUR OF HEAVY METALS IN MARINE ORGANISMS

(a) Absorptionfrom solution

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zinc in seawater (parts/106)

Absorptionby individual tissues also appearsto involve sorption at sites on and

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(b) Absorptionfrom food or ingestedparticles

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(i) Zinc in Carcinusmaenas

(ii) Lead in Crassostreavirginica

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I3 I 111111i t 1?Igt a11,h

zinc inr seawater (parts/106)

(iii) Laminaria digitata and Fucus vresicullosus

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i-3 1072 lo 1 100

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0 200 400 600~~~~~~6

distance from holdfast/mrn

(iv) Nereis diversicolor

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TABLE 3. METALS IN NEREIS DIVERSICOLOR FROMTWO ESTUARINE

4. DETRIMENTAL EFFECTS OF HEAVY METALS

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10-1 100 101 102

(b) Factors influencing toxicity

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(c) Sublethal effects

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(ii) Inhibitory effects

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copper in seawater (part/106) time/days

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(d) Basic effects

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