Cadmium - environmental aspects (EHC 135, 1992)

INTERNATIONAL PROGRAMME ON CHEMICAL SAFETY

ENVIRONMENTAL HEALTH CRITERIA 135

CADMIUM - ENVIRONMENTAL ASPECTS

This report contains the collective views of an international group of
experts and does not necessarily represent the decisions or the stated
policy of the United Nations Environment Programme, the International
Labour Organisation, or the World Health Organization.

Published under the joint sponsorship of
the United Nations Environment Programme,
the International Labour Organisation,
and the World Health Organization

First draft prepared by Dr S. Dobson,
Institute of Terrestrial Ecology, United Kingdom

World Health Orgnization
Geneva, 1992

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WHO Library Cataloguing in Publication Data

Cadmium : environmental aspects.

(Environmental health criteria ; 135)

1.Cadmium - toxicity 2.Environmental exposure
I.Series

ISBN 92 4 157135 7 (NLM Classification: QV 290)
ISSN 0250-863X

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CONTENTS

ENVIRONMENTAL HEALTH CRITERIA FOR CADMIUM - ENVIRONMENTAL ASPECTS

1. SUMMARY

2. IDENTITY, PHYSICAL AND CHEMICAL PROPERTIES, AND ANALYTICAL
METHODS

2.1. Physical and chemical properties
2.2. Analytical procedures
2.2.1. Sampling and preparation
2.2.2. Quantitative instrumental methods

3. NATURAL OCCURRENCE AND SOURCES OF ENVIRONMENTAL CONTAMINATION

3.1. Natural occurrence
3.2. Industrial uses
3.3. Sources of environmental cadmium
3.3.1. Sources of atmospheric cadmium
3.3.2. Sources of aquatic cadmium
3.3.3. Sources of terrestrial cadmium
3.4. Environmental transport and distribution
3.4.1. Atmospheric deposition
3.4.2. Transport from water to soil
3.5. Concentrations in various biota
3.5.1. Concentrations in fish
3.5.2. Concentrations in sea-birds
3.5.3. Concentrations in sea mammals
3.6. Concentrations adjacent to highways
3.7. Concentrations from industrial sources

4. KINETICS AND METABOLISM

4.1. Uptake
4.1.1. Uptake from water by aquatic organisms
4.1.1.1 Microorganisms
4.1.1.2 Aquatic molluscs
4.1.1.3 Other aquatic invertebrates
4.1.1.4 Fish
4.1.1.5 Model aquatic ecosystems
4.1.1.6 Uptake from aquatic sediment
4.1.1.7 Uptake from food relative to uptake from
water
4.1.2. Uptake by terrestrial organisms
4.1.2.1 Uptake into plants
4.1.2.2 Terrestrial invertebrates
4.1.2.3 Birds
4.2. Distribution
4.2.1. Aquatic organisms

4.2.2. Terrestrial organisms
4.2.2.1 Terrestrial plants
4.2.2.2 Terrestrial invertebrates
4.3. Elimination
4.4. Bioaccumulation and biomagnification

5. TOXICITY TO MICROORGANISMS

5.1. Aquatic microorganisms
5.1.1. Freshwater microorganisms
5.1.2. Estuarine and marine microorganisms
5.2. Soil and litter microorganisms

6. TOXICITY TO AQUATIC ORGANISMS

6.1. Toxicity to aquatic plants
6.2. Toxicity to aquatic invertebrates
6.2.1. Acute and short-term toxicity
6.2.1.1 Effects of temperature and salinity on
acute toxicity
6.2.1.2 Effect of water hardness
6.2.1.3 Effect of organic materials and sediment
6.2.1.4 Lifestage sensitivity
6.2.1.5 Other factors affecting acute and
short-term toxicity
6.2.2. Long-term toxicity
6.2.3. Reproductive effects
6.2.4. Physiological and biochemical effects
6.2.5. Behavioural effects
6.2.6. Interactions with other chemicals
6.2.7. Tolerance
6.2.8. Model ecosystems
6.3. Toxicity to fish
6.3.1. Acute and short-term toxicity
6.3.2. Reproductive effects and effects on early life
stages
6.3.3. Metabolic, biochemical and physiological effects
6.3.4. Structural effects and malformations
6.3.5. Behavioural effects
6.3.6. Interactions with other chemicals
6.4. Toxicity to amphibia

7. TOXICITY TO TERRESTRIAL ORGANISMS

7.1. Toxicity to terrestrial plants
7.1.1. Toxicity to plants grown hydroponically
7.1.2. Toxicity to plants grown in soil
7.1.3. In vitro physiological studies
7.2. Toxicity to terrestrial invertebrates
7.3. Toxicity to birds
7.3.1. Acute and short-term toxicity
7.3.2. Reproductive effects

7.3.3. Physiological effects
7.3.4. Behavioural effects
7.4. Toxicity to wild small mammals

8. EFFECTS IN THE FIELD

8.1. Tolerance
8.2. Effects close to industrial sources and highways
8.3. Effects on fish
8.4. Effects on sea-birds

9. EVALUATION

9.1. General considerations
9.2. The aquatic environment
9.3. The terrestrial environment

10. RECOMMENDATIONS FOR PROTECTING THE ENVIRONMENT

11. FURTHER RESEARCH

REFERENCES

APPENDIX 1

APPENDIX 2

APPENDIX 3

APPENDIX 4

APPENDIX 5

RESUME

RESUMEN

WHO TASK GROUP ON ENVIRONMENTAL HEALTH CRITERIA FOR CADMIUM -
ENVIRONMENTAL ASPECTS

Members

Dr L.A. Albert, Consultores Ambientales Asociados, S.C., Xalapa,
Veracruz, Mexico

Dr J.K. Atherton, Toxic Substances Division, Directorate for Air,
Climate and Toxic Substances, Department of the Environment,
London, United Kingdom

Dr R.W. Elias, Trace Metal Biogeochemistry, Environmental Criteria and
Assessment Office, US Environmental Protection Agency, Research
Triangle Park, North Carolina, USA

Dr A.H. El-Sebae, Faculty of Agriculture, Alexandria University,
Alexandria, Egypt

Dr R. Koch, Bayer AG, Leverkusen, Germany

Professor Y. Kodama, Department of Environmental Health, University of
Occupational and Environmental Health, Japan School of Medicine,
Yahata Nishi-ku, Kitakyushu City, Japan

Dr P. Pärt, Department of Zoophysiology, Uppsala University, Uppsala,
Sweden

Dr J.H.M. Temmink, Department of Toxicology, Agricultural University,
Wageningen, The Netherlands ( Chairman)

Secretariat

Dr S. Dobson, Institute of Terrestrial Ecology, Monks Wood
Experimental Station, Abbots Ripton, Huntingdon, Cambridgeshire,
United Kingdom ( Rapporteur)

Dr M. Gilbert, International Programme on Chemical Safety, World
Health Organization, Geneva, Switzerland ( Secretary)

Mr P.D. Howe, Institute of Terrestrial Ecology, Monks Wood
Experimental Station, Abbots Ripton, Huntingdon, Cambridgeshire,
United Kingdom

NOTE TO READERS OF THE CRITERIA DOCUMENTS

Every effort has been made to present information in the criteria
documents as accurately as possible without unduly delaying their
publication. In the interest of all users of the Environmental Health
Criteria documents, readers are kindly requested to communicate any
errors that may have occurred to the Director of the International
Programme on Chemical Safety, World Health Organization, Geneva,
Switzerland, in order that they may be included in corrigenda.

* * *

A detailed data profile and a legal file can be obtained from the
International Register of Potentially Toxic Chemicals, Palais des
Nations, 1211 Geneva 10, Switzerland (Telephone No. 7988400 or
7985850).

ENVIRONMENTAL HEALTH CRITERIA FOR CADMIUM - ENVIRONMENTAL ASPECTS

A WHO Task Group on Environmental Health Criteria for Cadmium -
Environmental Aspects met at the Institute of Terrestrial Ecology
(ITE), Monks Wood, United Kingdom, from 13 to 17 May 1991. Dr M.
Roberts, Director, ITE, welcomed the participants on behalf of the
host institution and Dr M. Gilbert opened the meeting on behalf of the
three cooperating organizations of the IPCS (UNEP/ILO/WHO). The Task
Group reviewed and revised the draft criteria document and made an
evaluation of the risks for the environment from exposure to cadmium.

The first draft of this document was prepared by Dr S. Dobson
(ITE). Dr M. Gilbert and Dr P.G. Jenkins, both members of the IPCS
Central Unit, were responsible for the technical development and
editing, respectively.

The efforts of all who helped in the preparation and finalization
of the document are gratefully acknowledged.

ABBREVIATIONS

ALAD delta-aminolevulinic acid dehydratase

DPTA diaminopropanoltetraacetic acid

EDTA ethylenediaminetetraacetic acid

EEC European Economic Community

EIFAC European Inland Fisheries Advisory Commission of FAO

FAO Food and Agriculture Organization of the United Nations

GESAMP Group of Experts on the Scientific Aspects of Marine
Pollution

MATC maximum acceptable toxicant concentration

NOEL no-observed-effect level

NTA nitrilotriacetic acid

NTEL no-toxic-effect level

1. SUMMARY

Cadmium (atomic number 48; relative atomic mass 112.40) is a
metallic element belonging, together with zinc and mercury, to group
IIb of the periodic table. Some cadmium salts, such as the sulfide,
carbonate, and oxide, are practically insoluble in water; these can be
converted to water-soluble salts in nature. The sulfate, nitrate, and
halides are soluble in water. The speciation of cadmium in the
environment is of importance in evaluating the potential hazard.

The average cadmium content of sea water is about 0.1 µg/litre or
less. River water contains dissolved cadmium at concentrations of
between < 1 and 13.5 ng/litre. In remote, uninhabited areas, cadmium
concentrations in air are usually less than 1 ng/m³. In areas not
known to be polluted, the median cadmium concentration in soil has
been reported to be in the range of 0.2 to 0.4 mg/kg. However, much
higher values, up to 160 mg/kg soil, are occasionally found.

Environmental factors affect the uptake and, therefore, the toxic
impact of cadmium on aquatic organisms. Increasing temperature
increases the uptake and toxic impact, whereas increasing salinity or
water hardness decreases them. Freshwater organisms are affected by
cadmium at lower concentrations than marine organisms. The organic
content of the water generally decreases the uptake and toxic effect
by binding cadmium and reducing its availability to organisms.
However, there is evidence that some organic matter may have the
opposite effect.

Cadmium is readily accumulated by many organisms, particularly by
microorganisms and molluscs where the bioconcentration factors are in
the order of thousands. Soil invertebrates also concentrate cadmium
markedly. Most organisms show low to moderate concentration factors of
less than 100. Cadmium is bound to proteins in many tissues. Specific
heavy-metal-binding proteins (metallothioneins) have been isolated
from cadmium-exposed organisms. The concentration of cadmium is
greatest in the kidney, gills, and liver (or their equivalents).
Elimination of the metal from organisms probably occurs principally
via the kidney, although significant amounts can be eliminated via the
shed exoskeleton in crustaceans. In plants, cadmium is concentrated
primarily in the roots and to a lesser extent in the leaves.

Cadmium is toxic to a wide range of microorganisms. However, the
presence of sediment, high concentrations of dissolved salts or
organic matter all reduces the toxic impact. The main effect is on
growth and replication. The most affected of soil microorganisms are
fungi, some species being eliminated after exposure to cadmium in
soil. There is selection for resistant strains after low exposure to
the metal in soil.

The acute toxicity of cadmium to aquatic organisms is variable,
even between closely related species, and is related to the free ionic
concentration of the metal. Cadmium interacts with the calcium
metabolism of animals. In fish it causes hypocalcaemia, probably by

inhibiting calcium uptake from the water. However, high calcium
concentrations in the water protect fish from cadmium uptake by
competing at uptake sites. Zinc increases the toxicity of cadmium to
aquatic invertebrates. Sublethal effects have been reported on the
growth and reproduction of aquatic invertebrates; there are structural
effects on invertebrate gills. There is evidence of the selection of
resistant strains of aquatic invertebrates after exposure to cadmium
in the field. The toxicity is variable in fish, salmonids being
particularly susceptible to cadmium. Sub-lethal effects in fish,
notably malformation of the spine, have been reported. The most
susceptible life-stages are the embryo and early larva, while eggs are
the least susceptible. There is no consistent interaction between
cadmium and zinc in fish. Cadmium is toxic to some amphibian larvae,
although some protection is afforded by sediment in the test vessel.

Cadmium affects the growth of plants in experimental studies,
although no field effects have been reported. The metal is taken up
into plants more readily from nutrient solutions than from soil;
effects have been mainly shown in studies involving culture in
nutrient solutions. Stomatal opening, transpiration, and
photosynthesis have been reported to be affected by cadmium in
nutrient solutions.

Terrestrial invertebrates are relatively insensitive to the toxic
effects of cadmium, probably due to effective sequestration mechanisms
in specific organs.

Terrestrial snails are affected sublethally by cadmium; the main
effect is on food consumption and dormancy, but only at very high dose
levels. Birds are not lethally affected by the metal even at high
dosage, although kidney damage occurs.

Cadmium has been reported in field studies to be responsible for
changes in species composition in populations of microorganisms and
some aquatic invertebrates. Leaf litter decomposition is greatly
reduced by heavy metal pollution, and cadmium has been identified as
the most potent causative agent for this effect.

2. IDENTITY, PHYSICAL AND CHEMICAL PROPERTIES, AND ANALYTICAL METHODS

2.1 Physical and chemical properties

Cadmium (atomic number 48; relative atomic mass 112.40) is a
metallic element belonging, together with zinc and mercury, to group
IIb in the periodic table. It is rarely found in a pure state. It is
present in various types of rocks and soils and in water, as well as
in coal and petroleum. Among these natural sources, zinc, lead, and
copper ore are the main sources of cadmium.

Cadmium can form a number of salts. Its mobility in the
environment and effects on the ecosystem depend to a great extent on
the nature of these salts. Since there is no evidence that
organocadmium compounds, where the metal is covalently bound to
carbon, occur in nature, only inorganic cadmium salts will be
discussed. Cadmium may occur bound to proteins and other organic
molecules and form salts with organic acids, but in these forms, it is
regarded as inorganic.

Cadmium has a relatively high vapour pressure. The vapour is
oxidized quickly to produce cadmium oxide in the air. When reactive
gases or vapour, such as carbon dioxide, water vapour, sulfur dioxide,
sulfur trioxide or hydrogen chloride, are present, the vapour reacts
to produce cadmium carbonate, hydroxide, sulfite, sulfate or chloride,
respectively. These salts may be formed in stacks and emitted to the
environment.

Some of the cadmium salts, such as the sulfide, carbonate or
oxide, are practically insoluble in water. However, these can be
converted to water-soluble salts in nature under the influence of
oxygen and acids; the sulfate, nitrate, and halogenates are soluble in
water. The physical and chemical properties of cadmium and its salts
are summarized in Table 1. Equilibrium data for complexes of group IIB
cations, comparing cadmium with zinc and mercury, can be found in
Table 2. A diagrammatic representation of the capacity of soil types
for metals is given in Fig. 1.

The speciation of cadmium in soil water (Fig. 2) and surface
water (Fig. 3) is important for the evaluation of its potential
hazard.

Most of the cadmium found in mammals, birds, and fish is probably
bound to protein molecules.

Table 1. Physical and chemical properties of cadmium and its salts

Cadmium Cadmium Cadmium Cadmium Cadmium Cadmium Cadmium Cadmium
chloride acetate oxide hydroxide sulfide sulfate sulfite

CAS number 7440-43-9 10108-64-2 543-90-8 1306-19-0 1306-23-6 10124-36-4

Empirical formula Cd CdCl₂ C₄H₆CdO₄ CdO Cd(OH)₂ CdS CdSO₄ CdSO₃

Relative atomic or
molecular mass 112.41 183.32 230.50 128.40 146.41 144.46 208.46 192.46

Relative density 8.642 4.047 2.341 6.95 4.79 4.82 4.691

Melting point (°C) 320.9 568 256 < 1426 300 1750 1000 decomposes
(decomposes)

Boiling point (°C) 765 960 decomposes 900-1000
(decomposes)

Water solubility insoluble 1400 very soluble insoluble 0.0026 0.0013 755 slightly soluble
(g/litre) (20 °C) (26 °C) (18 °C) (0 °C)

Table 2. Equilibrium data for complexes of group IIB cations ^a

System Metal log K₁ DELTA H₁ DELTA S₁
(kJ mol^-1) (J K^-1 mol^-1)

zinc 5.0 ^b 0 ^b 105
M²⁺-OH_- cadmium 3.9 ^b 0 79
mercury 10.6 ^b - -

zinc 0.8 7.5 42
M²⁺-F^- cadmium 0.6 4.2 25
mercury 1.0 ^c 4.2 ^c 33 ^c

zinc - 0.2 5.4 16
M²⁺-Cl^- cadmium 1.5 - 0.4 29
mercury 7.1 - 24.3 54

zinc - 0.6 1.7 - 4
M²⁺-Br^- cadmium 1.7 - 4.2 21
mercury 9.4 - 40.1 46

zinc - 1.5 - -
M²⁺-I^- cadmium 2.1 - 9.2 8
mercury 12.9 ^c - 75.3 ^c - 8 ^c

zinc 5.3 - -
M²⁺-CN^- cadmium 5.6 - 30.5 ^b 13 ^b
mercury 18.0 ^c - 96 ^b 0 ^b

zinc 0.7 ^d - 5.9 ^d - 4 ^d
M²⁺-SCN^- cadmium 1.3 ^d - 9.6 ^d - 8^d
mercury 9.1 ^d - 49.7 ^d 8

zinc 1.9 - -
M²⁺-S₂O₃^{2- e} cadmium 4.7 - 6.3 ^d 67 ^d
mercury 29.9 ^d - -

zinc 2.4 ^f - 10.9 ^f 8 ^f
M²⁺-NH₃ cadmium 2.7 ^f - 14.6 ^f 4 ^f
mercury 8.8 ^f - -

zinc 4.8 ^c - 11.3 ^g 59 ^g
²⁺ - cadmium 4.1 ^d - 8.8 ^b 50 ^g
(glycinate)^- mercury 10.3 ^c - -

zinc 16.4 - 20.5 247
M²⁺-(EDTA)^4- cadmium 16.4 - 38.1 184
mercury 21.5 - 79.0 146

^a From: Aylett (1979). Data, which refer to first stepwise stability
constant, [ML]/[M][L], unless otherwise stated, are from Sillen
(1964) and Smith & Martell (1974, 1975, 1976); see also Christensen
et al. (1975). All values refer to measurements in water at 25 °C;
the ionic strength is 3 mol/litre unless otherwise stated.
^b ionic strength 0
^c ionic strength 0.5 mol/litre
^d ionic strength 1.0 mol/litre
^e Data refer to overall stability constant, ß₂ = [ML₂]/[M][L]²
^f ionic strength 2.0 mol/litre
^g ionic strength 0.1 mol/litre

2.2 Analytical procedures

The following is an outline of the analytical procedure for
cadmium; further information is given in Environmental Health Criteria
134: Cadmium (WHO, 1992).

2.2.1 Sampling and preparation

Only a few nanograms, or even less, of cadmium may be present in
collected samples of air or water, whereas hundreds of micrograms may
be present in small samples of kidney, sewage sludge, and plastics.
Different techniques are, therefore, required for the collection,
preparation, and analysis of the samples.

In general, the techniques available for measuring cadmium in the
environment and biological materials cannot differentiate between
cadmium species. With special separation techniques,
cadmium-containing proteins can be isolated and identified. In most
studies, the concentration or amount of cadmium in water, air, soil,
plants, and other environmental or biological material is determined
as the element.

Standard trace element methods can generally be used for the
collection of samples (LaFleur, 1976; Behne, 1980). During the
handling and storage of samples, particularly liquid samples, special
care must be taken to avoid contamination; coloured materials in
containers, especially plastics and rubber, should be avoided. Glass
and transparent, cadmium-free polyethylene, polypropylene or teflon
containers are usually considered suitable for storing samples. All
containers and glassware should be precleaned in dilute nitric acid
and deionised water. In order to avoid possible adsorption of cadmium
onto the container wall, water samples or standards with low cadmium
concentrations should not be stored for long periods of time.

To prepare samples for analysis, inorganic solid samples (such as
soil or dust samples) are usually dissolved in an acid, e.g., nitric
acid. Organic samples need to be subjected to wet ashing (digested) or
dry ashing. When the cadmium concentration is low, special treatment
is sometimes needed. The procedures for separating cadmium from
interfering compounds and concentrating the samples are very important
steps in obtaining accurate results.

2.2.2 Quantitative instrumental methods

The most commonly used methods, at present, are atomic absorption
spectrometry, electrochemical methods, neutron activation analysis,
atomic emission spectrometry, atomic fluorescence spectrometry and
proton-induced X-ray emissions (PIXE) analysis. Analytical methods for
cadmium have been reviewed by Friberg et al. (1986). Detection limits
of some of the methods are given in Table 3.

Table 3. Analytical procedures ^a

Method Detection limit Matrix

Atomic absorption 1 to 5 mg/litre water
spectrometry
0.1 mg/kg biological samples

electrothermal a few pg
atomization

Electrochemical method
(potentiometric stripping
analysis) 0.1 mg/litre urine

Neutron activation 0.1 to 1 mg/litre biological
analysis samples/fluids

X-ray atomic 17 mg/kg biological samples
fluorescence

^a From: Friberg et al. (1986)

3. NATURAL OCCURRENCE AND SOURCES OF ENVIRONMENTAL CONTAMINATION

3.1 Natural occurrence

A comparison of natural and anthropogenic sources of trace metals
is given in the Appendix 1.

Cadmium is widely distributed in the earth's crust at an average
concentration of about 0.1 mg/kg and is commonly found in association
with zinc. However, higher levels are present in sedimentary rocks:
marine phosphates often contain about 15 mg/kg (GESAMP, 1984).
Weathering and erosion result in the transport by rivers of large
quantities of cadmium to the world's oceans and this represents a
major flux of the global cadmium cycle; an annual gross input of 15
000 tonnes has been estimated (GESAMP, 1987).

In background areas away from ore bodies, surface soil
concentrations of cadmium typically range between 0.1 and 0.4 mg/kg
(Page et al., 1981). The median cadmium concentration in non-volcanic
soil ranges from 0.01 to 1 mg/kg, but in volcanic soil levels of up to
4.5 mg/kg have been found (Korte, 1983).

Volcanic activity is a major natural source of atmospheric
cadmium release. The global annual flux from this source has been
estimated to be 100-500 tonnes (Nriagu, 1979). Deep sea volcanism is
also a source of environmental cadmium release, but the role of this
process in the global cadmium cycle remains to be quantified.

The average cadmium content of sea water is about 0.1 µg/litre or
less (Korte, 1983), while river water (Mississippi, Yangtze, Amazon,
and Orinoco sampled between 1976 and 1982) contains dissolved cadmium
at concentrations of < 1.1-13.5 ng/litre (Shiller & Boyle, 1987).
Cadmium levels of up to 5 mg/kg have been reported in river and lake
sediments and from 0.03 to 1 mg/kg in marine sediments (Korte,1983).

Current measurements of dissolved cadmium in surface waters of
the open oceans give values of < 5 ng/litre. The vertical
distribution of dissolved cadmium in ocean waters is characterized by
a surface depletion and deep water enrichment, which corresponds to
the pattern of nutrient concentrations in these areas (Boyle et al.,
1976). This distribution is considered to result from the absorption
of cadmium by phytoplankton in surface waters and its transport to the
depths, incorporation to biological debris, and subsequent release. In
contrast, cadmium is enriched in the surface waters of areas of
upwelling and this also leads to elevated levels in plankton
unconnected with human activity (Martin & Broenkow, 1975; Boyle et
al., 1976). Oceanic sediments underlying these areas of high
productivity can contain markedly elevated cadmium levels as a result
of inputs associated with biological debris (Simpson, 1981).

In remote, uninhabited areas, cadmium concentrations in air are
usually less than 1 ng/m³ (Korte,1983).

3.2 Industrial uses

The principal applications of cadmium fall into five categories:
protective plating on steel; stabilizers for PVC; pigments in plastics
and glass; electrode material in nickel-cadmium batteries; and as a
component of various alloys (Wilson, 1988).

The relative importance of the major applications has changed
considerably over the last 25 years. The use of cadmium for
electroplating represented in 1960 over half the cadmium consumed
worldwide, but in 1985 its share was less than 25% (Wilson, 1988).
This decline is usually linked to the introduction of stringent
effluent limits from plating works and, more recently, to the
introduction of general restrictions on cadmium consumption in certain
countries. In contrast, the use of cadmium in batteries has shown
considerable growth in recent years from only 8% of the total market
in 1970 to 37% by 1985. The use of cadmium in batteries is
particularly important in Japan and represented over 75% of the total
consumption in 1985 (Wilson, 1988).

Pigments and stabilizers accounted for 22% and 12% of the total
world consumption in 1985. The share of the market by cadmium pigments
remained relatively stable between 1970 and 1985 but the use of the
metal in stabilizers during this period showed a considerable decline,
largely as a result of economic factors. The use of cadmium as a
constituent of alloys is relatively small and has also declined in
importance in recent years, accounting for about 4% of total cadmium
use in 1985 (Wilson, 1988).

3.3 Sources of environmental cadmium

3.3.1 Sources of atmospheric cadmium

Estimates of cadmium emissions to the atmosphere from human and
natural sources have been carried out at the worldwide, regional, and
national level; examples of such inventories are shown in Table 4.

The median global total emission of the metal from human sources
in 1983 was 7570 tonnes (Nriagu & Pacyna, 1988) and represented about
half the total quantity of cadmium produced in the same year. In both
the European Economic Community (EEC) and on a worldwide scale
(Nriagu, 1989), about 10-15% of total airborne cadmium emissions arise
from natural processes, the major source being volcanic action.

Municipal refuse contains cadmium derived from discarded
nickel-cadmium batteries and plastics containing cadmium pigments and
stabilizers. The incineration of refuse is a major source of
atmospheric cadmium release at country, regional, and worldwide level
(Table 4).

Steel production can also be considered as a waste-related
source, as large quantities of cadmium-plated steel scrap are recycled

by this industry. As a result, steel production is responsible for
considerable emissions of atmospheric cadmium.

3.3.2 Sources of aquatic cadmium

Non-ferrous metal mines represent a major source of cadmium
release to the aquatic environment. Contamination can arise from mine
drainage water, waste water from the processing of ores, overflow from
the tailings pond, and rainwater run-off from the general mine area.
The release of these effluents to local watercourses can lead to
extensive contamination downstream of the mining operation. Mines
disused for many years can still be responsible for the continuing
contamination of adjacent watercourses (Johnson & Eaton, 1980).

At the global level, the smelting of non-ferrous metal ores has
been estimated to be the largest human source of cadmium release to
the aquatic environment (Nriagu & Pacyna, 1988). Discharges to fresh
and coastal waters arise from liquid effluents produced by air
pollution control (gas scrubbing) together with the site drainage
waters.

Table 4. Estimates of atmospheric cadmium emissions (tonnes/year) on a national, regional and worldwide basis

Source United EEC ^b Worldwide ^c
Kingdom ^a

Natural sources ND 20 150-2600 ^d

Non-ferrous metal
production

mining ND ND 0.6-3
zinc and cadmium 20 920-4600
copper 3.7 6 1700-3400
lead 7 39-195

Secondary production ND 2.3-3.6

Production of cadmium-containing
substances ND 3 ND

Iron and steel production 2.3 34 28-284

Fossil fuel combustion

coal 1.9 6 176-882
oil 0.5 41-246

Refuse incineration 5 31 56-1400

Sewage sludge incineration 0.2 2 3-36

Table 4 (contd).

Source United EEC^b Worldwide ^c
Kingdom ^a

Phosphate fertilizer manufacture ND ND 68-274

Cement manufacture 1 ND 8.9-534

Wood combustion ND ND 60-180

TOTAL EMISSIONS 14 130 3350-14 640

^a From: Hutton & Symon (1986); data apply to 1982-1983
^b From: Hutton (1983); data apply to 1979-1980 (the EEC consisted,
at that time, of Belgium, Denmark, Federal Republic of Germany,
Italy, Luxembourg, The Netherlands, Republic of Ireland, and the
United Kingdom)
^c From: Nriagu & Pacyna (1988); data apply to 1983
^d From: Nriagu (1979)
ND Not determined

The manufacture of phosphate fertilizer results in a
redistribution of the cadmium present in the rock phosphates between
the phosphoric acid product and gypsum waste. In many cases, the
gypsum is disposed of by dumping in coastal waters, which leads to
considerable cadmium inputs. Some countries, however, recover the
gypsum for use as a construction material and thus have negligible
cadmium discharges (Hutton, 1982).

The atmospheric fallout of cadmium to fresh and marine waters
represents a major input of cadmium at the global level (Nriagu &
Pacyna, 1988). A GESAMP study of the Mediterranean Sea indicated that
this source is comparable in magnitude to the total river inputs of
cadmium to the region (GESAMP, 1985). Similarly, large cadmium inputs
to the North Sea (110-430 tonnes/year) have also been estimated, based
on the extrapolation from measurements of cadmium deposition along the
coast (van Alst et al., 1983a,b). However, another approach based on
model simulation yielded a modest annual cadmium input of 14 tonnes
(Krell & Roeckner, 1988).

Acidification of soils and lakes may result in enhanced
mobilization of cadmium from soils and sediments and lead to increased
levels in surface and ground waters (WHO Working Group, 1986).

3.3.3 Sources of terrestrial cadmium

Solid wastes are disposed of in landfill sites, resulting in
large cadmium inputs at the national and regional levels when
expressed as total tonnage (Hutton, 1982; Hutton & Symon, 1986).

Sources include the ashes from fossil fuel combustion, waste from
cement manufacture, and the disposal of municipal refuse and sewage
sludge.

Of greater potential environmental significance are the solid
wastes from both non-ferrous metal production and the manufacture of
cadmium-containing articles, as well as the ash residues from refuse
incineration. These three waste materials are characterized by
elevated cadmium levels and as such require disposal to controlled
sites to prevent the contamination of the ground water.

The agricultural application of phosphate fertilizers represents
a direct input of cadmium to arable soils. The cadmium content of
phosphate fertilizers varies widely and depends on the origin of the
rock phosphate. It has been estimated that fertilizers of West African
origin contain 160-255 g cadmium/tonne of phosphorus pentoxide, while
those derived from the southeastern USA contain 35 g/tonne (Hutton,
1982).

The annual rate of cadmium input to arable land from phosphate
fertilizers has been estimated at 5 g/ha for the countries of the EEC
(Hutton 1982). This only represents about 1% of the surface soil
cadmium burden. Despite the relatively small size of this input,
long-term continuous application of phosphate fertilizers has been
shown to cause increased soil cadmium concentrations (Williams &
David, 1973, 1976; Andersson & Hahlin, 1981).

The application of municipal sewage sludge to agricultural soils
as a fertilizer can also be a significant source of cadmium; a value
of 80 g/ha has been estimated for the United Kingdom (Hutton & Symon,
1986). On a national or regional basis, however, these inputs are much
smaller than those from either phosphate fertilizers or atmospheric
deposition (see section 3.4).

Polluted soils can contain cadmium levels of up to 57 mg/kg (dry
weight) resulting from sludge applied to soil and up to 160 mg/kg in
the vicinity of metal-processing industry (Fleischer et al., 1974).
The highest cadmium levels reported appear to be from ancient mining
areas with levels of up to 468 mg/kg.

3.4 Environmental transport and distribution

3.4.1 Atmospheric deposition

Cadmium is removed from the atmosphere by dry deposition and by
precipitation. In rural areas of Scandinavia, annual deposition rates
of 0.4-0.9 g/ha have been measured (Laamanen, 1972; Andersson, 1977).
Similarly, in a rural region of Tennessee, USA, a deposition rate of
0.9 g/ha was observed (Lindberg et al., 1982). Hutton (1982) suggested
that 3 g/ha per year was a representative value for the atmospheric
deposition of cadmium to agricultural soils in rural areas of the EEC.

The corresponding input for these areas from the application of
phosphate fertilizers is 5 g/ha per year (see section 3.3).

Many industrial sources of cadmium possess tall stacks which
bring about the wide dispersion and dilution of particulate emissions.
Nevertheless, cadmium deposition rates around smelter facilities are
often markedly elevated nearest the source and generally decrease
rapidly with distance (Hirata, 1981). Soil cadmium concentrations in
excess of 100 mg/kg are commonly encountered close to long established
smelters (Buchauer, 1972).

Crop plants growing near to atmospheric sources of cadmium may
contain elevated cadmium levels (Carvalho et al., 1986). However, it
is not always possible to distinguish whether the cadmium is derived
directly from surface deposition or originates from root uptake, since
soil levels in such areas are generally higher than normal.

3.4.2 Transport from water to soil

Rivers contaminated with cadmium can contaminate surrounding
land, either through irrigation for agricultural purposes, by the
dumping of dredged sediments, or through flooding (Forstner, 1980;
Sangster et al., 1984). For example, agricultural land adjacent to the
Neckar River, Germany, received dredged sediments to improve the soil,
a practice that produced soil cadmium concentrations in excess of 70
mg/kg (Forstner, 1980).

Much of the cadmium entering fresh waters from industrial sources
is rapidly adsorbed by particulate matter, where it may settle out or
remain suspended, depending on local conditions. This can result in
low concentrations of dissolved cadmium even in rivers that receive
and transport large quantities of the metal (Yamagata & Shigematsu,
1970)

3.5 Concentrations in various biota

Table 5 indicates the levels of cadmium found in various biota
(Eisler, 1985).

Eisler (1985) concluded that there are at least six trends
evident from the abundant residue data available for cadmium.

* Marine organisms generally contain higher cadmium residues than
their freshwater and terrestrial counterparts.

* Cadmium tends to concentrate in the viscera of vertebrates,
especially the liver and kidneys.

* Cadmium concentrations are generally higher in older organisms.

* Higher cadmium residues are generally associated with industrial
and urban sources, although this does not apply to sea birds and
sea mammals.

* Cadmium residues in plants are normally less than 1 mg/kg.
However, plants growing in soil amended with cadmium (e.g., from
sewage sludge) may contain significantly higher levels.

* The species analysed, season of collection, ambient cadmium
levels, and the sex of the organism probably all affect the
residue level.

Table 5. Concentrations of cadmium in biota

Organisms Parts of the Cadmium concentration
organisms (mg/kg dry weight)

Marine organisms

Algae < 1 to 16

Molluscs soft parts up to 425
kidney up to 547
liver up to 782
digestive gland up to 1163

Crustaceans whole body < 0.4-6.2

Annelids whole body 0.1-3.6

Fish whole body up to 5.2

Birds kidney up to 231

Mammals kidney up to 300

Freshwater organisms

Plants whole plant 0.5-1.8
roots up to 6.7

Molluscs soft parts; fresh weight 0.2-1.4

Annelids whole body; fresh weight 0.5-3.2

Fish whole body; fresh weight 0.01-1.04

Table 5 (contd).

Organisms Parts of the Cadmium concentration
organisms (mg/kg dry weight)

Terrestrial organisms

Plants whole plant up to 27.1
grain up to 257

Annelids whole body 3-12.6

Birds whole body; fresh weight < 0.05-0.24
kidney; fresh weight up to 7.4

Mammals kidney up to 8.1

3.5.1 Concentrations in fish

May & McKinney (1981) monitored freshwater fish from the USA in
1976 and 1977 and found cadmium concentrations ranging from 0.01 to
1.04 mg/kg (wet weight), the mean being 0.085 mg/kg. This represented
a significant decline from the mean 1972 concentration of 0.112 mg/kg.
The authors pointed out that this decline parallels a decline in
cadmium metal production and consumption over the same period.

Hardisty et al. (1974a) sampled flounder ( Platichthyes flesus)
from the Severn estuary, United Kingdom, and found mean cadmium
concentrations of 3.4-7.3 mg/kg (dry weight). No overall correlation
between cadmium concentration and length or age was observed, although
the largest (27-29 cm) and the oldest („ 5 years) fish gave the
highest mean concentrations. Hardisty et al. (1974b) found a positive
correlation between the cadmium content of a variety of fish species
and the crustacea content of their diet. Lovett et al. (1972) sampled
fish from New York State, USA, and reported mean cadmium
concentrations of < 10-142.7 µg/kg (fresh weight). There was no
relationship between total residues and size, sex or age of lake trout
( Salvelinus namaycush).

3.5.2 Concentrations in sea-birds

Cadmium has been found in a wide variety of birds, and
particularly high levels have been reported in pelagic sea-birds. Much
of the cadmium occurs in the kidney and liver, and relatively little
is transferred to the eggs. A review of the uptake of cadmium and of
the factors that affect it can be found in Scheuhammer (1987).
Interestingly, the concentrations of cadmium in sea-birds are often
higher in areas with little or no contamination from industrial
sources (Bull et al., 1977; Hutton, 1981; Osborn & Nicholson, 1984).

3.5.3 Concentrations in sea mammals

High levels of cadmium have been reported in sea mammals from
areas around the world, which they are assumed to take up from their
diet of fish. Roberts et al. (1976) showed that kidney levels of
cadmium in the common seal off the United Kingdom coast were age
related. Drescher et al. (1977) showed a similar relationship in seals
off the German coast and Hamanaka et al. (1982) in stellar sea lions
off the coast of Japan. Similar trends in dolphins and porpoises have
been reported (Falconer et al., 1983; Honda & Tatsukawa, 1983; Honda
et al., 1986). Muir et al. (1988) sampled white-beaked dolphins
( Lagenorhynchus albirostris) and pilot whales ( Globicephala
melaena) from the coast of Newfoundland, Canada, and reported mean
cadmium levels in kidney (dry weight) of 13.6 mg/kg and 108 mg/kg,
respectively. Cadmium concentrations were age related in pilot whales.
The lower levels found in dolphins were probably related both to
species differences and to the fact that they were all young animals.

3.6 Concentrations adjacent to highways

Muskett & Jones (1980) monitored levels of cadmium adjacent to a
heavily used road. The concentrations in air were highest at a
distance from the road of 0-10 m, and a similar pattern was found in
soil. Cadmium levels in earthworms sampled at known distances from a
highway revealed levels of 12.6 mg/kg (dry weight) within 3 m falling
to 7.1 mg/kg approximately 50 m from the highway. The level in
earthworms from control sites was 3 mg/kg (Gish & Christensen, 1973).
The land snail Cepaea hortensis accumulates cadmium from roadside
verges (Williamson, 1980). The highest concentration of cadmium was
found in the digestive gland (40.3 mg/kg dry weight) and kidney (12.8
mg/kg dry weight). There was little metal in the head and foot, which
make up most of the body tissue. The author showed that age accounted
for 80% of the total variance of soft tissue body burdens. The cadmium
body burdens were found to be effectively immobile, accumulating
progressively with age.

3.7 Concentrations from industrial sources

Burkitt et al. (1972) analysed the cadmium content of ryegrass at
various distances from a zinc smelter and found 50, 10.8, and 1.8
mg/kg dry weight at distances of 0.3, 1.9, and 11.3 km, respectively,
from the smelter.

Teraoka (1989) found that cadmium levels in rice roots were
significantly higher in industrial urban and roadside areas of Japan
compared to sparsely populated areas. The mean level in industrial
areas was 10 mg/kg (dry weight).

Beyer et al. (1985) monitored biota from the vicinity of two zinc
smelters in eastern Pennsylvania, USA. Cadmium concentrations were
highest in carrion insects (25 mg/kg dry weight), followed by fungi
(9.8 mg/kg), leaves (8.1 mg/kg), shrews (7.3 mg/kg), moths (4.9

mg/kg), mice (2.6 mg/kg), songbirds (2.5 mg/kg), and berries (1.2
mg/kg).

Van Hook (1974) sampled soil and earthworms from soil that had
not been disturbed for 30 years and reported mean cadmium levels in
the soils and earthworms of 0.35 and 5.7 mg/kg dry weight,
respectively. Ma et al. (1983) analysed soil and earthworms
( Lumbricus rubellus) at varying distances from a zinc-smelting
plant. Cadmium concentrations ranged from 0.1 to 5.7 mg/kg for the
soil and 20 to 202 mg/kg for the worms, and there was a correlation
between decreasing distance from the smelter and increasing cadmium
levels. Pietz et al. (1984) sampled soil and earthworms ( Aporrectodea
tuberculata) and ( Lumbricus terrestris) from mine soil and
non-mine soil, either amended or not with sewage sludge. Soil and
worms from mine soil gave residues of 0.6 and 3.8 mg/kg dry weight,
respectively, in non-amended soil and 2 and 22 mg/kg in sludge-amended
soil. Residues in soil and worms from non-mined soil were 1 and 12
mg/kg for non-amended and 3.5 and 36 mg/kg for sludge-amended soil,
respectively. The much lower capacity of worms from areas already
contaminated with cadmium to take up the metal suggests some selection
for varieties that control metal uptake. Morgan & Morgan (1988)
sampled earthworms ( Lumbricus rubellus and Dendrodrilus rubidus)
from one uncontaminated site and fifteen metal-contaminated sites (in
the vicinity of disused non-ferrous metalliferous mines) in the United
Kingdom. Cadmium concentrations in the worms ranged from 8 mg/kg (dry
weight) to 1786 mg/kg; they were generally higher than soil levels,
and the total soil cadmium explained 82% to 86% of the variability in
earthworm cadmium concentrations. The authors found some evidence that
cadmium accumulation was suppressed in extremely organic soils.

Martin et al. (1980) reported cadmium levels in a variety of
invertebrates sampled from sites contaminated by airborne cadmium. The
woodlouse was shown to accumulate cadmium principally in the
hepatopancreas.

Van Straalen & van Wensem (1986) analysed 13 species of
arthropods from an area polluted by zinc factory emissions. They found
no effect of body size or trophic level on the cadmium content of the
arthropods.

Roberts & Johnson (1978) sampled invertebrates and their diet
from the area of an abandoned lead-zinc mine in the United Kingdom.
They found cadmium levels higher in herbivorous invertebrates than in
the vegetation on which they fed (but not markedly so). There were
much higher levels of cadmium in carnivorous invertebrates, suggesting
that cadmium might have a capacity for accumulation in food chains.

In contrast to mercury levels, total cadmium body burdens were
higher in sparrows ( Passer domesticus) caught in industrialised
areas of Poland than in those caught in agricultural regions (Pinowska
et al., 1981). Pigeon brain, liver, and kidney sampled in rural,

suburban, and urban areas gave a good indication of the level of
environmental pollution with cadmium (Hutton & Goodman, 1980).

Hunter & Johnson (1982) monitored small mammals near to an
industrial works complex and found that cadmium accumulated
particularly in the liver and kidney. Cadmium levels in the liver
ranged rom 1.5 to 280 mg/kg (dry weight) and in the kidney from 7.4 to
193 mg/kg. Small mammals from unpolluted sites contained liver levels
ranging from 0.5 to 25 mg/kg and kidney levels of 1.5-26 mg/kg. The
insectivorous common shrew ( Sorex areneus) was found to be a more
prominent accumulator of cadmium than omnivorous and herbivorous small
mammals, based on body burden to dietary metal concentration ratios.
Similar results were obtained by Andrews et al. (1984) who monitored
cadmium levels in the herbivorous short-tailed field vole ( Microtus
agrestis) and the insectivorous common shrew ( S. araneus) from a
revegetated metalliferous mine site. Mean cadmium concentrations were
1.84 mg/kg (dry weight) and 52.7 mg/kg for voles and shrews,
respectively, values that were significantly higher than those found
in control sites.

4. KINETICS AND METABOLISM

Appraisal

In aquatic systems, cadmium is most commonly taken up by
organisms directly from water, but may also be ingested with
substantially contaminated food. The free metal ion, Cd²⁺, is the
form most available to aquatic species. Uptake from water may be
reduced by the concentration of calcium and magnesium salts (water
hardness). Cadmium uptake from sea water may be greatly reduced by
the formation of less available complexes with chloride. Organic
complexes with cadmium can be classified in three groups: those that
are unavailable (e.g., EDTA, NTA, DPTA), those that are available but
less so than the free Cd²⁺ (e.g., fulvic acids of low relative
molecular mass), and those that form readily available hydrophobic
complexes with cadmium (xanthates and dithiocarbamates).

Organisms in the freshwater environment are contaminated
according to their ability to absorb or adsorb cadmium from the
water, rather than to their position in the food chain. Consequently,
differences in cadmium concentration between species at the same
trophic level are common and there is no evidence for
biomagnification. Conversely, marine organisms take up cadmium
principally from food. The primary source of cadmium in terrestrial
systems is the soil, and uptake follows the typical food chain
pathway, although deposition of cadmium on plant and animal surfaces
can account for some additional contamination at each trophic level.
Variations in uptake and retention occur, and there is some evidence
for biomagnification in carnivores. Organisms that feed on sediment
or detritus may accumulate more cadmium than those in the grazing
food chain. High levels of cadmium have been reported in sea mammals,
pelagic sea-birds, and terrestrial invertebrates.

Within a variety of organisms, cadmium is distributed throughout
most tissues, but tends to accumulate in the roots, gills, livers,
kidneys, hepatopancreas, and exoskeleton. Cadmium in the cell is
often bound to cytoplasmic proteins, a possible detoxifying
mechanism. Elimination probably occurs primarily via the kidney but
also via moulting of the exoskeleton.

There is some evidence of an interaction between cadmium and
other metals, especially calcium and zinc. Cadmium may replace
calcium on the calcium-specific protein calmodulin and is affected by
other physiological processes that regulate the uptake of calcium. In
certain circumstances, zinc increases cadmium retention in the liver
and kidneys of aquatic vertebrates. In terrestrial systems, high soil
zinc levels can reduce cadmium uptake appreciably.

Selection can lead to cadmium-tolerant populations in both the
aquatic and terrestrial environments.

4.1 Uptake

4.1.1 Uptake from water by aquatic organisms

Several studies have shown that the free metal ion, Cd²⁺, is
the form of cadmium most available to aquatic organisms (Sunda et al.,
1978; Borgmann, 1983; Part et al., 1985; Sprague, 1985).

Inorganic cadmium complexes appear not to be taken up, at least
by fish (Part et al., 1985). This is particularly important in marine
water where cadmium is mainly present in soluble chloride complexes
(Zirino & Yamamoto 1972). It is most probable that chloride
complexation is responsible for the reduced cadmium accumulation and
toxicity in a variety of organisms observed with increasing salinities
(Coombs, 1979).

In the case of organic cadmium complexes, the chemical properties
are of importance with respect to bioavailability. Three categories
can be distinguished. The first comprises cadmium complexes with EDTA,
NTA, and DPTA, which are unavailable to aquatic organisms (Sunda et
al., 1978; Part & Wikmark, 1984). The second consists of complexes
that to some extent contribute to the total metal uptake, i.e. uptake
is higher than predicted from the actual Cd²⁺ activity, but the
complex is still less available than the free Cd²⁺ ion. This group
includes fulvic acids of low relative molecular mass (Giesy et al.,
1977; John et al., 1987), the amino acid histidine (Pecon & Powell,
1981), and carboxylic acids like citric acid (Guy & Ross Kean, 1980;
Part & Wikmark, 1984). The third category includes compounds such as
xanthates and dithiocarbamates that form hydrophobic complexes with
heavy metals. These hydrophobic complexes act as metal carriers across
biological membranes and they lead to a greater uptake of cadmium in
aquatic organisms than when the metal is present as the free ion
(Poldoski, 1979; Block & Part, 1986; Gottofrey et al., 1988; Block,
1991). This latter observation is of particular environmental concern
because xanthates are used in the mining industry in the enrichment of
metals from sulfide ores by flotation. Xanthate concentrations of
between 4 and 400 µg/litre have been measured in waters receiving
effluent from metal refineries (enrichment plants) (Waltersson, 1984).

Another water quality parameter affecting cadmium uptake is the
Ca²⁺ and Mg²⁺ concentration (hardness) of the water. Increasing
Ca²⁺ concentration reduces cadmium uptake through fish gills (Part
et al., 1985; Wicklund, 1990), cadmium accumulation (Carroll et al.,
1979), and cadmium toxicity for fish (Calamari et al., 1980). Two
mechanisms can be distinguished for the Ca²⁺-mediated reduction in
cadmium uptake. The first is an inhibitory effect on uptake into gill
tissue, while the second is related to the adaptive response of the
fish to increased Ca²⁺ concentrations (Calamari et al., 1980,
Wicklund 1990). Mg²⁺ also reduces cadmium uptake through fish gills
but at 5 times higher concentrations than Ca²⁺ (Part et al., 1985).

Cadmium uptake in fish is not strongly pH dependent; uptake in
rainbow trout gills was not affected over the pH range 5-7 (Part et
al., 1985).

Recent data from fish gills indicate that, to some extent, Cd²⁺
shares uptake mechanisms with Ca²⁺; these two ions are about the
same size and also form complexes with the same kind of ligands. Thus
Cd²⁺ can replace Ca²⁺ in the calcium-specific protein calmodulin
(Flik et al., 1987). In the gills, Cd²⁺ is assumed to enter the
epithelial cells down its concentration and electrical gradient by
facilitated diffusion through a calcium channel in the apical membrane
(Verbost et al., 1989). Several lines of evidence support this
assumption. Firstly, increasing water Ca²⁺ concentrations reduce
cadmium uptake. Secondly, cadmium in the water inhibits Ca²⁺ uptake
in the gills (Verbost et al., 1987; Reid & McDonald, 1988). Thirdly,
La³⁺, a calcium channel blocker in cell membranes, inhibits both
Ca²⁺ and Cd²⁺ uptake in the gills. Fourthly, the hypocalcaemic
hormone stanniocalcin reduces both Ca²⁺ and Cd²⁺ uptake in the
gills (Verbost et al., 1989). Stanniocalcin has been shown to close
the apical calcium channel in the gill epithelial cells thereby
reducing Ca²⁺ uptake from the water (Lafeber et al., 1988). The
hormone is secreted when the fish has a surplus of Ca²⁺, i.e.
hypercalcaemic. The two-fold effect of Ca²⁺ on cadmium uptake in
fish discussed previously can be well explained by this model. A
direct competition between Ca²⁺ and Cd²⁺ at the apical calcium
channel reduces the uptake of cadmium into the cells, while the
adaptive response in Ca²⁺-rich water probably involves an increased
stanniocalcin level, which closes the apical calcium/cadmium channel.

The transport mechanism from the epithelial cells to the blood is
unclear. Cadmium is not transported by the high affinity Ca-ATPase in
the basolateral epithelial membrane which transports Ca²⁺ (Verbost
et al., 1988). The possible involvement of the Na⁺/Ca²⁺ exchange
mechanism, where Cd²⁺ replaces Ca²⁺, has recently been suggested
as a translocation mechanism to the blood (personal communication to
the IPCS by G. Flik).

Zinc also has been shown to reduce cadmium uptake through the
gills (Wicklund, 1990). Like cadmium, zinc is assumed to enter the
epithelial cell by facilitated diffusion (Spry & Wood, 1989) and,
furthermore, Ca²⁺ acts antagonistically on zinc uptake.

Taken together, these data suggest that the apical epithelial
membrane of fish gills contains an ion channel shared by cadmium and
calcium, and probably also zinc. The movement of metals through this
channel is controlled both by external factors such as the Ca²⁺
content of the water and internal factors such as hormones.

Increasing temperature increases the uptake of cadmium from water
(Vernberg et al., 1974; Zaroogian & Cheer, 1976; Denton &
Burdon-Jones, 1981).

4.1.1.1 Microorganisms

In the alga Chlorella pyrenoidosa, uptake of cadmium was
completely blocked by 0.2 mg manganese/litre and inhibited by 2 to 5
mg iron/litre, but calcium, magnesium, molybdenum, copper, zinc, and
cobalt had no effect on uptake (Hart & Scaife, 1977).

Cultures of Chlorella accumulate twice as much cadmium at pH
7.0 as at pH 8.0 when exposed to 0.5 mg cadmium/litre (Hart & Scaife,
1977).

4.1.1.2 Aquatic molluscs

Hardy et al. (1984) found greater uptake of cadmium from sea
water into oysters given an uncontaminated phytoplankton food source
than into those without food. The authors explain their findings on
the basis that the presence of phytoplankton increases the flow of
water through the oysters. Studies on oysters without a food source
may thus underestimate cadmium uptake. Oysters fed phytoplankton
containing cadmium retained only 0.59% of this cadmium; the majority
of the cadmium in molluscs is taken up directly from the water. The
oyster accumulates about twice as much cadmium in summer as in the
winter. This is presumed to reflect the increased flow of water
through the animal at higher temperatures (Zaroogian & Cheer, 1976).

Hardy et al. (1981) showed that clams ( Protothaca staminea)
took up much less cadmium from water in the presence of sediment at
3.6 g/litre. The uptake was only 17% of that measured in sediment-free
water.

Langston & Zhou (1987a,b) found no evidence of cadmium uptake
into the bivalve Macoma balthica involving metallothionein or
metallothionein-like proteins. Accumulation in soft tissues was linear
throughout a 29-day exposure period, whereas uptake onto the shell was
characterized as saturation kinetics. In contrast, the gastropod
Littorina littorea did show induction of specific cadmium-binding
proteins, which contributed to uptake and storage of cadmium.

Watling & Watling (1983) demonstrated uptake of cadmium in a
dose-dependant manner into sandy beach gastropod molluscs in
laboratory experiments. Much of the cadmium (as chloride) accumulated
in the gill. The rate of cadmium uptake was 0.01 mg/kg per day for
Donax serra and 0.16 mg/kg per day for the smaller Bullia
rhodostoma after exposure to cadmium at 20 µg/litre. The freshwater
snail Physa integra took up more cadmium as exposure increased,
concentrations ranging between 1 and 40 µg/litre. The highest
concentration factors were found with the lowest exposure
concentration (Spehar et al., 1978a). Wier & Walter (1976) exposed the
freshwater snail Physa gyrina to 1.3 mg cadmium/litre (as the
chloride) and found an average cadmium uptake rate of 0.55 mg/kg per

hour over 24 h. Heavier snails took up less cadmium, after the same
exposure, than lighter individuals.

4.1.1.3 Other aquatic invertebrates

Rainbow & White (1989) investigated uptake of cadmium and zinc in
three marine crustaceans, Palaemon elegans (Decapoda),
Echinogammarus pirloti (Malacostraca), and Elminius modestus
(Cirripedia) at water concentrations of cadmium between 0.5 and 1000
µg/litre and zinc between 2.5 and 4000 µg/litre. All three crustaceans
accumulated the non-essential cadmium at all dissolved cadmium
concentrations without regulation. Differences between species were
interpreted by the authors in terms of differences in cuticle
permeability and way of life. All three species took up zinc more
rapidly than cadmium; the ratios between molar uptake rates of zinc to
cadmium were 11.4:1, 2.7:1, and 3.7:1 for the three species,
respectively, following an exposure to a molar ratio of 1.7:1.

4.1.1.4 Fish

Cadmium uptake in fish continues for some considerable time in
fish exposed to the metal. The peak of tissue residues may not be
reached for several weeks, particularly after exposure to low
concentrations of the metal (Cearley & Coleman, 1974; Benoit et al.,
1976; Sullivan et al., 1978a).

Douben (1989a) exposed the stone loach Noemacheilus barbatulus
to cadmium in water (as the sulfate) at a concentration of 1 mg/litre
and monitored uptake and loss at different temperatures with fed and
starved fish. The size of the fish affected both uptake and loss of
cadmium, bioconcentration factors decreasing with size. Uptake of
cadmium increased with temperature up to about 16 °C and decreased as
the concentration of cadmium in the water increased. Feeding the fish
increased the rate of uptake of cadmium from the water. The author
concluded that metabolic rate was an important factor in the uptake of
cadmium into the fish and in its subsequent loss.

4.1.1.5 Model aquatic ecosystems

Ferard et al. (1983) investigated the transfer of cadmium through
a model food-chain consisting of an alga, a daphnid, and a fish.
Concentration factors relative to food were low, indicating that
cadmium is mainly taken up directly from water. Daphnids fed algae
containing cadmium at between 4.5 and 570 mg/kg dry weight showed a
maximum concentration factor of 1. Fish fed contaminated daphnids or
algae showed concentration factors of 0.0038 and 0.0018, respectively.
Nimmo et al. (1977) reported low concentration factors, ranging from
0.018 to 0.027, for grass shrimp fed on brine shrimp containing
cadmium at between 27 and 182 mg/kg. Rehwoldt & Karimian-Teherani
(1976) fed zebrafish on food containing cadmium acetate at 10 mg/kg
over a period of 6 months. Maximum residues, in males and females
respectively, were 5.92 and 13.64 mg/kg, the median residue levels

after 6 months of exposure being 5.19 and 12.95 mg/kg (on a dry weight
basis).

4.1.1.6 Uptake from aquatic sediment

Ray et al. (1980b) exposed the ragworm Nereis virens to
sediment to which cadmium chloride had been added. Smaller worms took
up more cadmium relative to body weight than larger worms. The cadmium
was taken up in a dose-related manner and no equilibrium was reached
during the 24-day experiment. The rate of uptake directly from sea
water also increased with exposure concentration over the range of
0.03 to 9.2 mg/litre. For the range of sediment cadmium concentrations
used (1 to 4 mg/kg), the corresponding concentrations in the overlying
sea water were 0.03 to 0.1 mg/litre. Comparing uptake into the
ragworms from water with these concentrations to the uptake from the
spiked sediment produced identical concentrations of cadmium in the
worms. Rate of uptake from sediment was between 16 and 39 times less
than the uptake from the corresponding exposure to cadmium in water.
The authors concluded that all of the uptake of cadmium from sediment
derived from desorbed metal ions in the interstitial water.

4.1.1.7 Uptake from food relative to uptake from water

Fish can take up cadmium from the surrounding water and from
ingested food. The main uptake route in fresh water is from the water
via the gills (Williams & Giesy, 1978). However, the relative
importance of food and water to the body burden depends very much on
the cadmium content of the food organism. In contaminated areas with
an increased cadmium content in food organisms, the relative
importance of food as a cadmium source may increase. In the marine
environment, where cadmium is mainly present in chloride complexes not
available to fish, the relative importance of food as a cadmium source
increases. Consequently food has been shown to be the main cadmium
source in marine fish (Pentreath, 1977; Dallinger et al., 1987).

4.1.2 Uptake by terrestrial organisms

4.1.2.1 Uptake into plants

The uptake of cadmium into plants generally depends upon the
availability of the metal in soil solution. The soil pH and
composition, particularly the nature of soil clays, the organic matter
content, and, obviously, the soil cadmium level, affect this
availability. The relationship between soil cadmium level and plant
uptake is not a simple one because of the wide variety of soil
characteristics that affect the extent of cadmium uptake. Cataldo &
Wildung (1978), Peterson & Alloway (1979), and Page et al. (1981) have
reviewed this subject.

Plants grown in a greenhouse or a container take up more cadmium
than the same plants grown in soil with the same cadmium levels in the
field. This is due to greater root development in a confined volume in

containers and to the fact that all the roots are in contact with
cadmium-contaminated soil. In the field, roots may grow down below the
cadmium-contaminated level (Page & Chang, 1978; De Vries & Tiller,
1978).

Mahler et al. (1978) cultured lettuce and chard on acid or
calcareous soils to which cadmium sulfate had been added at levels up
to 320 mg/kg. For both types of soil there was a dose-related uptake
of cadmium from soil into leaves. The uptake of the metal was much
greater in acid than in calcareous soils, particularly at higher rates
of cadmium application (over 40 mg/kg). At the highest soil
concentration of 320 mg/kg, lettuce leaves contained cadmium at a
concentration of 800 mg/kg and chard leaves 1600 mg/kg when grown in
acid soil. Leaves of lettuce cultured on calcareous soils with cadmium
at 320 mg/kg contained a lower cadmium concentration of 200-300 mg/kg
and chard, similarly cultured, contained 300 mg/kg or less. Bingham et
al. (1980) showed an effect of soil pH on cadmium (as sulfate) uptake
in rice; more metal was incorporated as acidity increased. Chaney et
al. (1975) reported that liming of soil in which soybeans were growing
decreased the concentrations of cadmium in leaves from 33 to 5 mg/kg
dry weight as pH increased from 5.3 to 7.0. Eriksson (1988)
investigated the effect of pH on the uptake of cadmium into perennial
ryegrass ( Lolium perenne) and winter rape ( Brassica napus). The
more soluble fractions of cadmium in soil increased as the pH was
lowered; increasing the pH from 5 to 7 with calcium oxide invariably
reduced the cadmium content of ryegrass plants, but this decrease was
less consistent when the pH was increased from 5 to 6. The cadmium
content of rape plants was markedly higher at pH 4 than pH 5. Adding
more cadmium to the soil increased the amount of cadmium in the plants
in direct proportion to the increased concentration of the metal in
soil over the range 0 to 5 mg/kg. Eriksson (1988) found that soil
organic matter decreased the availability of cadmium to perennial
ryegrass and winter rape grown in pots. Addition of organic material
to sand and clay soils reduced cadmium uptake to a greater extent in
the sand.

When Mitchell & Fretz (1977) cultured seedlings of three species
of tree (red maple, white pine, and Norway spruce) hydroponically or
in soil with added cadmium, the concentration in roots was greater
than that in leaves. Cadmium added to soil was less readily taken up
than cadmium added to nutrient solutions. Similarly, Root et al.
(1975) reported greater cadmium concentration in roots than in shoots
of maize grown hydroponically in a medium containing cadmium chloride.
Harkov et al. (1979) found the highest uptake of cadmium into
hydroponically grown tomatoes in the roots, while stems had lower
cadmium concentrations than leaves.

Lepp et al. (1987) measured high concentrations of cadmium in the
sporophores (fruiting bodies) of the fungus Amanita muscaria growing
in birch woodland. The fungus sporophores contained 29.9 mg/kg dry
weight, compared to a cadmium level of 0.4 mg/kg in the soil on which
they grew. The cadmium was released from the rotting sporophore, after

it had shed its spores, in a form which was readily available to other
plants growing on the woodland soil; this was shown experimentally
with lettuce plants grown in pots. The authors calculated that an
abundant population of sporophores could recycle 1.4% of the total
cadmium load in leaf litter to higher plants over a period of 14 days
(the mean lifespan of the sporophores).

4.1.2.2 Terrestrial invertebrates

Beyer et al. (1982) demonstrated that earthworms concentrated
cadmium from soils amended with sewage sludge containing cadmium
oxide. Cadmium concentrations were as high as 100 mg/kg in worms
exposed to soils containing cadmium at 2 mg/kg, a concentration factor
of 50. Adding calcium carbonate to soils decreased the cadmium uptake
of worms slightly, while high soil zinc levels decreased the cadmium
uptake appreciably. Results were variable with different sludge
treatments. Hartenstein et al. (1980) amended sludge with 10, 50, and
100 mg/kg cadmium (as cadmium sulfate) and added earthworms ( Eisenia
foetida). The worms accumulated 3.9, 2.04, and 1.44 times the
respective sludge levels of cadmium over a period of 5 weeks. In field
trials on non-amended soils containing 12 to 27 mg cadmium/kg, worms
sampled during a 28-week period gave levels of cadmium ranging from 8
to 46 mg/kg.

Terrestrial pulmonate snails retained up to 59% of cadmium
administered in their diet as the chloride (Russell et al., 1981). The
highest retention was after dosing at 25 mg cadmium/kg diet. The
higher the dose (up to 1000 mg/kg diet) the lower the percentage
retention of the metal. Ireland (1981) noted that in the terrestrial
slug Arion ater most of the cadmium was located in the digestive
gland without association with any particular sub-cellular organelles,
and isolated a specific cadmium-binding protein from the animals.

4.1.2.3 Birds

In a study by White & Finley (1978), adult mallard ducks were fed
a diet containing cadmium chloride at levels of 2, 20 or 200 mg/kg and
killed at 30-day intervals. The cadmium content increased with dose
level and time (except in the case of the highest dose where body
burden peaked after 60 days), and the highest concentrations occurred
in the liver and kidney. The highest levels overall occurred after
dosing for 60 days at 200 mg/kg; cadmium concentrations were 109 mg/kg
in the liver and 134 mg/kg in the kidney.

Nicholson & Osborn (1983) dosed starlings ( Sturnus vulgaris)
with cadmium chloride at a concentration of 2 mg/kg body weight, three
times weekly for 6 weeks, and reported a wide range of kidney
concentrations (from < 10 to > 200 mg/kg dry weight).

4.2 Distribution

4.2.1 Aquatic organisms

In higher organisms, cadmium can be bound in several different
tissues, whereas in plants cadmium is bound to the cell wall in roots.

Brooks & Rumsby (1967) measured the cadmium taken up by the
oyster ( Ostrea sinuata) from water containing ¹¹⁵Cd (50 mg/litre).
The soft parts of the oyster contained 100 mg cadmium/kg after 100 h.
Concentrations in tissues were, in decreasing order, 360 mg/kg for
gills, 285 mg/kg for heart, 141 mg/kg for the visceral mass, 83 mg/kg
for the mantle, 53 mg/kg for white muscle, and 25 mg/kg for striated
muscle.

Nimmo et al. (1977) reported that in the pink shrimp the
hepatopancreas took up more cadmium than other tissues. Lower
concentrations were found in the exoskeleton, muscle, and serum.
Short-term exposure of the crab Uca pugilator to cadmium chloride
led to the hepatopancreas and gill concentrations of the metal being
similar after a 24-h exposure to 1 mg cadmium/litre (Vernberg et al.,
1974).

Sangalang & Freeman (1979) determined the cadmium in tissues of
brook trout exposed to the metal (added as the chloride) via the water
or by injection. After water exposure to cadmium chloride at 1
µg/litre, the trout showed greatest uptake of the metal in the gills,
kidney, and liver. The gills and the posterior kidney revealed a
higher metal content than any other tissues. Levels of cadmium in
whole blood and plasma, heart, spleen, testis, stomach, and skin were
higher than control levels after 77 and 93 days of exposure. Smith et
al. (1976) found the greatest accumulation of the metal in the kidney
of catfish exposed to cadmium (as sulfate) in the water. In an
autoradiographic study of cadmium distribution in rainbow trout
exposed to cadmium in water, Tjalve et al. (1986) confirmed the
general picture of cadmium distribution, the metal being found in the
gills, liver, and kidney. However, they also observed heavy labelling
of the olfactory rosette and the olfactory nerve, an observation not
reported earlier. In a detailed study they later showed that cadmium
was transported axonally from the olfactory rosette to the bulbus
olfactorius but not further into the brain (Gottofrey, 1990). The
significance of this observation with respect to the olfactory
responses of fish in cadmium-contaminated environments remains to be
investigated.

The few studies that have been conducted on the subcellular
distribution of cadmium indicate that, while much is located in the
cytosol, a significant proportion can be found in the nucleus and the
mitochondria. Cadmium is bound in the cytosol to proteins of low
relative molecular mass, metallothioneins, and other cadmium-binding

proteins. These proteins are rich in the sulfur-containing amino acid
cysteine but poor in aromatic amino acids.

Metallothioneins have been isolated and characterized in a number
of aquatic and terrestrial organisms. Fish metallothioneins have
received considerable interest in recent years as tools in monitoring
metal pollution in the environment (Hamilton & Mehrle, 1986; Hogstrand
& Haux, 1990a). Simple methods to analyse fish metallothionein have
been developed, including differential pulse polarography (Olson &
Haux, 1986) and radioimmunoassay based on specific antibodies to fish
metallothionein (Hogstrand & Haux, 1990b). Olson & Haux (1986) found
a strong correlation between hepatic metallothionein and cadmium
accumulation in perch collected from cadmium-contaminated water.

4.2.2 Terrestrial organisms

4.2.2.1 Terrestrial plants

Jones & Johnston (1989) analysed cereal grain and herbage from
long-term experimental plots at Rothamsted, United Kingdom, and found
that uptake of cadmium into herbage was greatest where phosphate
fertilizer had been applied. It was also greater from unlimed soils
than from limed soils. However, the authors concluded that there was
little evidence of a long-term (1840-1986) increase in crop cadmium
concentrations.

Byrne et al. (1976) analysed higher fungi from Slovenia,
Yugoslavia, and found levels of cadmium ranging from 0.53 to 39.9
mg/kg dry weight (average 5.0 mg/kg). This is an order of magnitude
higher than in most other plants. Although the fungi were collected
from industrial, urban, and uncontaminated sites, the levels found in
the fungi were not very different between sites. The authors suggested
geological rather than industrial sources for the cadmium in these
soils.

The high uptake by mushrooms and related species is probably due
to a cadmium-binding phosphoglycoprotein, cadmium-myco-phosphatin,
which has been isolated from the mushroom Agaricus macrosporus
(Meisch & Schmitt, 1986).

4.2.2.2 Terrestrial invertebrates

Hopkin & Martin (1985) investigated the storage of cadmium in the
woodlouse Oniscus asellus from heavily contaminated woodland 3 km
downwind from a smelter. The hepatopancreas was found to contain up to
5 g cadmium/kg dry weight without apparent ill effects upon the
organism. Cadmium was reported to be stored intracellularly in the
copper- and sulfur-containing granules of epithelial S cells. In a
later study (Hopkin, 1990) it was found that considerable interspecies
differences exist with regard to storage in the hepatopancreas.
Oniscus asellus stored five times more cadmium than Porcello scaber
under the same conditions. The carnivorous centipede Lithobius

variegatus, when fed on cadmium-contaminated hepatopancreas from
woodlice, accumulated cadmium which was likewise stored in the midgut
(Hopkin & Martin, 1984).

Berger & Dallinger (1989) studied the distribution of cadmium
between several organs of the terrestrial snail Arianta arbustorum
during a 20-day feeding experiment on cadmium-enriched agar. Of the
cadmium in the medium, 54% was taken up, of which 66% was distributed
to the hepatopancreas, leading to a concentration of more than 500
mg/kg dry weight. In other organs (intestine, foot/mantle, gonads),
the cadmium concentration was considerably lower.

In the earthworm Lumbricus rubellus taken from heavy-metal-
polluted soil, more than 70% of the cadmium burden was found in the
posterior alimentary canal (Morgan & Morgan, 1990). This distribution
prevented dissemination of large concentrations of cadmium into other
tissues and, according to the authors, may represent a detoxification
strategy.

4.3 Elimination

Information on loss of cadmium from organisms is relatively
scarce. The information that does exist suggests that this is very
variable, and has been reviewed by Coombs (1979) and Taylor (1983).
Organisms that accumulate cadmium also tend to retain the metal for
long periods. The main excretory route appears to be via the kidney,
except in the case of organisms that moult, where loss from the shed
exoskeleton can be significant.

Robinson & Wells (1975) administered a single oral dose of
cadmium acetate to softshell turtles ( Trionyx spinifer) and killed
and dissected the animals either 48 h or 96 h later. After 48 h, 9.43%
of the total dose was recovered from tissues, while turtles killed
after 96 h had retained 4.02% of the dose. The greatest retention of
cadmium, after both time periods, was in the liver. Cadmium was also
retained in the small intestine for the first 48 h, but the amount had
decreased by 96 h.

Harrison & Klaverkamp (1989) exposed rainbow trout ( Salmo
gairdneri) and lake whitefish (Coregonus clupeaformis) to cadmium in
water, via a continuous-flow system, or the diet, via pelleted food,
for 72 days. The fish were then kept in clean water on a cadmium-free
diet for a further 56 days. In the case of water-exposed fish, the
majority of the cadmium was present in the gill and kidney, but
food-exposed fish retained cadmium principally in the kidney, gut, and
liver. Bioconcentration factors for exposure via the water were 55 for
the trout and 42 for the whitefish, whereas concentration factors from
the food were less than 1 for both species. However, both species
accumulated a greater proportion of the cadmium that was in the food
than that in water (1% as against 0.1%). Equilibrium bioconcentration
factors were estimated to be 161 for trout and 51 for whitefish.

In the same model, the half-times for depuration of accumulated
cadmium ranged from 24 to 63 days. Douben (1989b) investigated the
kinetics of cadmium in freshwater fish (the stone loach Noemacheilus
barbatulus) exposed to cadmium via the diet (tubifex worms
previously contaminated with cadmium by uptake from water). The body
burden of cadmium declined after the period of feeding with
contaminated diet more rapidly in starved than in fed fish. Rate
constants for loss of cadmium appeared to be greater during the
exposure period than after exposure. Both uptake and loss of cadmium
were influenced by the body weight of the fish.

Janssen et al. (1991) investigated uptake and loss of cadmium
from contaminated soil by four species of soil arthropod and developed
kinetic models that gave good predictions of the degree of
accumulation in a variety of species. They also reviewed data on other
soil arthropods (Tables 6 and 7). The kinetics of cadmium in different
arthropods is related to taxonomy and reflects the different
physiological characteristics of the different organisms. Some,
notably isopods and molluscs, take up and retain cadmium in their
tissues with little or no excretion. These species are capable of
holding large quantities of the metal in the hepatopancreas without
apparent ill effect. There is no direct correlation between
assimilation capacity and the capacity to excrete or eliminate
cadmium. Figure 4 illustrates the uptake of cadmium (measured as total
body burden) and its subsequent loss in four species of arthropods.
Elimination half-lives of 53, 8, and 2 days, respectively, have been
reported for Platynothrus peltifer, Orchesella cincta, and
Notiophilus biguttatus; no elimination took place over 130 days in
Neobisium muscorum.

Sawicka-Kapusta et al. (1987) investigated the effect of keeping
the vole Clethrionomys glareolus at different temperatures on the
rate of loss of cadmium from body tissues. Although the different
temperatures (10 °C and 20 °C) affected the metabolic rate of the
voles, there was no difference in the rate of loss of cadmium.

4.4 Bioaccumulation and biomagnification

Bioaccumulation occurs when the concentration in the organism
exceeds the concentration in the nutrient medium and is expressed
quantitatively as a bioconcentration factor. Progressive
bioaccumulation at each trophic level is termed biomagnification.

Table 6. Cadmium assimilation efficiencies in different soil invertebrates

Species Food Cadmium concentration Assimilation efficiency Reference
in food (µmol/g) (%)

Snail
Arianta arbuslorum^a agar 1.48 55-92 Berger & Dallinger (1989) ^b

Centipede
Lithobius variegatus isopod 1.21-10.2 0-7.2 Hopkin & Martin (1984)
hepatopancreas

Millipede
Clomeris marginata maples leaves 8.2-40.6 Hopkin et al. (1985)

Pseudoscorpion
Neobisium muscorum collembolans 0.20 58.9 Janssen et al. (1991)

Mite
Platynothrus peltifer green algae 0.15 17.2 Janssen et al. (1991)

Insects
Orchesella cincta green algae 0.09 8.3 Van Straalen et al. (1987)
Orchesella cincta green algae 0.15 9.4 Janssen et al. (1991)
Notiophilus biguttatus collembolans 0.23 35.5 Janssen et al. (1991)

^a assimilation value for midgut gland
^b recalculated from the data

Table 7. Excretion constants (k) for cadmium in different soil invertebrates

Species Taxonomic k Reference
group (day^-1)

Helix pomatia snail 0 Dallinger & Wieser (1984) ^b

Cepaea nemoralis snail 0.007 Williamson (1980) ^b

Oniscus asellusa isopod 0.002 Hopkin (1989) ^b

Neobisium muscorum pseudoscorpion 0 Janssen et al. (1991)

Lycosa spp spider 0.007 Van Hook & Yates (1975)

Platynothrus peltifer oribatid mite 0.013 Janssen et al. (1991)

Orchesella cincta collembolan 0.061 Van Straalen et al. (1987)

Orchesella cincta collembolan 0.087 Janssen et al. (1991)

Acheta domesticus cricket 0.090- Van Hook & Yates (1975)
0.110

Notiophilus biguttatus carabid beetle 0.375 Janssen et al. (1991)

^a k value for midgut gland or hepatopancreas
^b recalculated from the data

Bioconcentration factors (the ratio between the cadmium
concentration in the organism and the concentration in the medium) for
several groups of organisms studied under laboratory conditions are
shown in Table 8. They range from 16 to 130 000 and do not seem to
show any consistent pattern.

Table 8. Bioconcentration of cadmium in laboratory studies

Organism Size Stat/ Organ ^a Temperature Duration Exposure Bioconcentration Reference
flow (°C) (days) (µg/litre) factor ^b

Freshwater alga 10 10 3000 dw ^c Ferard et al. (1983)
(Chlorella vulgaris)

Freshwater alga stat 20-22 14 250 4940 daw Cain et al. (1980)
(Scenedesmus obliquus)

Freshwater diatom flow WB 23 10 40 000 Conway (1978)
(Asterionella formosa)

Submerged plant WP 25 30 25 1730 dw Nakada et al. (1979)
(Elodea nuttallii)

Water hyacinth leaves 28 500 16 dw ^c Kay & Haller (1986)
(Eichhornia crassipes)

American oyster 4.9-5.1 g flow WB 16-20 21 10 116 ww Eisler et al. (1972)
(Crassostrea virginica) 4280 aw

8.1 g flow ST 2.8-22.6 280 5 2376 ww Zaroogian & Cheer (1976)
18 472 dw

Mussel 32-34 mm flow ST 13 166 10 50 802 dw Riisgard et al. (1987)
(Mytilus edulis)

Scallop 6.8-7.7 g flow WB 16-20 21 10 131 ww Eisler et al. (1972)
(Aquipecten irradians) 3970 aw

Bay scallop 0.51-0.73 g flow ST 9.5-16 42 60 20 400 Pesch & Stewart (1980)
(Argopecten irradians)

Crab 2-4 g WB 10 14 37 152 dw Ray et al. (1980a)
(Pandalas montagui)

Grass shrimp 20-33 mm flow WB 9.5-16 42 60 223 Pesch & Stewart (1980)
(Palaemonetes pugio)

Table 8 (contd).

Organism Size Stat/ Organ ^a Temperature Duration Exposure Bioconcentration Reference
flow (°C) (days) (µg/litre) factor ^b

Lobster 160-169 g flow WB 16-20 21 10 21 ww Eisler et al. (1972)
(Homarus americanus) 10 aw

Mummichog 2.3-2.4 g flow WB 16-20 21 10 15 ww Eisler et al. (1972)
(Fundulus heteroclitus) 200 aw

Fathead minnow flow WB 13.9-15.3 21 49 190 Sullivan et al. (1978a)
(Pimephales promelas)

Red maple leaves 15-27 45 0.5 14 400 dw ^d Mitchell & Fretz (1977)
(Acer rubrum) roots 15-27 45 0.5 131 800 dw ^d Mitchell & Fretz (1977)
leaves 15-27 101 2.6 mg/kg 0.76 dw ^e Mitchell & Fretz (1977)
roots 15-27 101 2.6 mg/kg 12.5 dw ^e Mitchell & Fretz (1977)

White pine leaves 15-27 66 0.5 3400 dw ^d Mitchell & Fretz (1977)
(Pinus strobus) roots 15-27 66 0.5 118 400 dw ^d Mitchell & Fretz (1977) leaves 15-27 36 52.6 mg/kg 1.2 dw ^e Mitchell & Fretz (1977)
roots 15-27 36 52.6 mg/kg 10.4 dw ^e Mitchell & Fretz (1977)

^a WB = whole body; WP = whole plant; ST = soft tissues
^b Chloride salt used unless stated otherwise; bioconcentration factor = concentration in the organism divided by concentration
in the medium; dw = dry weight; ww = wet weight; aw = ash weight; daw = dry ash weight
^c Nitrate salt used
^d The medium was a cadmium-enriched nutrient solution
^e The medium was a cadmium-amended soil mix

Microorganisms generally exhibit a high capacity to take up
cadmium from water and retain the metal in their cells. The highest
bioconcentration factors reported have been for micro-organisms, the
greatest value being 40 000 in a freshwater diatom (Conway, 1978). In
this diatom, 58% of the cadmium was located in the cellular content
with 25% in the organic coating of the frustule and 17% in the
silicaceous frustule. The bioconcentration factor of 3000 for the alga
Chlorella (Ferard et al., 1983) is typical of the value for
microorganisms. Flatau et al. (1988) demonstrated the uptake (it was
not specified whether this referred to absorption or adsorption) of
cadmium from sea water by marine bacteria; the uptake of the metal
increased with its concentration in the water, and the accumulation
rate was a logarithmic function of the dose. Sorption was only
observed with exposure concentrations above 10 µg Cd/litre, suggesting
that a threshold had to be exceeded for cadmium uptake to occur.
Dongmann & Nurnberg (1982) showed that the bioconcentration factor for
a marine diatom, Thalassiosira rotula, decreased with increasing
metal concentration, suggesting a saturation effect. Their reported
concentration factors, which vary between 1000 and 2000, reflect the
reduced sorption of cadmium by marine microorganisms compared with
their freshwater relatives. Hart & Scaife (1977) reported a direct
relationship between the level of cadmium in the medium and sorption
to the alga Chlorella exposed to cadmium concentrations ranging from
0.25 to 1.00 mg/litre.

After water hyacinths had been exposed for 4 weeks to water
containing 0.5 or 1.0 mg cadmium/litre, added as cadmium nitrate, the
leaves had accumulated 8.00 and 17.20 mg/kg, respectively (Kay &
Haller, 1986).

Molluscs concentrate cadmium to a high degree over a period of
time, but uptake is often slow. Oysters showed a concentration factor
of only 149 over a 10-day period (Eisler et al., 1972) but a factor of
2714 after 40 weeks (Zaroogian & Cheer, 1976). Elliott et al. (1985)
examined the accumulation of cadmium, copper, lead, and zinc in the
tissues of the mussel, Mytilus edulis. Under simultaneous exposure
to all four metals, both lead and cadmium were accumulated in direct
proportion to the exposure time, whereas copper and zinc were not.
Accumulation of cadmium was influenced by the presence of other
metals.

Compared with oysters, the related bay scallop shows greater
accumulation of cadmium when exposed to low concentration of the metal
as the chloride over 6 weeks (Pesch & Stewart, 1980). Short-term
exposure of the same scallop to higher concentrations of cadmium
resulted in very much lower concentration factors. Exposure for 96 h
to cadmium (as the chloride) at up to 2.0 mg/litre led to a
bioconcentration factor of around 50 (Nelson et al., 1976).

Bioconcentration factors (from water and food) and
biomagnification factors (from food alone) were calculated for the
freshwater isopod Assellus aquaticus by van Hattum et al. (1989).

Much of the cadmium (added as the chloride) was taken up from the
water (bioconcentration factor 18 000), but there was little uptake
from food (bioconcentration factor 0.08). Direct uptake from water
accounted for between 50 and 98% of the body burden after 30 days of
exposure (based on dry weight measures). Cadmium was readily taken up
by the isopod even at exposure concentrations of 1 µg/litre.
Experiments conducted at two different pHs (5.9 and 7.6) revealed no
significant effect of pH on uptake of cadmium by the isopod.

Wright & Frain (1981b) demonstrated that adult intermoult
amphipods ( Gammarus pulex) accumulated only half as much cadmium
from a solution of 5 mg/litre in the presence of 200 mg calcium/litre
as with 20 mg calcium/litre.

Ramamoorthy & Blumhagen (1984) investigated the uptake of
cadmium, mercury, and zinc by rainbow trout (Salmo gairdneri) in a
model system which simulated the presence of other competing
compartments that would be found in nature. The system consisted of
either a simple sediment/water model or a more complex series of
compartments in dialysis bags of suspended sediment, cation and anion
exchange resins (to represent naturally occurring polyelectrolyte
materials of plant origin), and fish. River water was used as the
fluid transfer medium, and the system was continuously stirred.
Equilibrium with one heavy metal ion did not inhibit the uptake of
other metal ions; cadmium and zinc were taken up after equilibrium
with mercury. The authors calculated approximate partition
coefficients (fish/substrate) to be 2.8 for sediment, 550 for water,
and 2 and 3.6 for the cation and anion exchange resins, respectively.

The problem of expressing changes in concentration between
trophic levels is that the units are not compatible. There is no
significance to a bioconcentration term that expresses a ratio of
cadmium in soil moisture to cadmium in plant tissue, or cadmium in
plant tissue to cadmium in herbivore tissue. Therefore, it is
difficult to assess the impact of cadmium on the environment in terms
of bioconcentration factors. An alternative method is to measure both
cadmium and calcium at each trophic level and express these
measurements as a molar ratio of these two elements. (The molar ratio
should be used to account for the movement by atoms, not grams.)
Differences between trophic levels are calculated as the ratio of the
higher trophic level to the lower. This approach, called
biopurification, recognizes that the flow of the non-nutrient cadmium
through successive trophic levels follows a pathway similar to that of
nutrients such as calcium, and that calcium must pass natural chemical
and physiological barriers, such as membranes and selective enzymes,
that progressively purify the pool of the nutrient calcium relative to
the non-nutrient cadmium. In the case where two similar ecosystems are
compared, and where one is believed to be more contaminated than the
other, the relative degree of contamination can be calculated as the
difference between molar ratios at the same or similar trophic levels.

It is unfortunate that the absence of concentration data on
nutrients such as calcium or, alternatively, zinc, prohibits the
calculation of biopurification factors for any of the studies
discussed in this monograph.

5. TOXICITY TO MICROORGANISMS

Appraisal

Cadmium is toxic to a wide range of microorganisms in culture
(effects of cadmium on microorganisms in the field are discussed in
chapter 8). However, the presence of sediment, organic matter or high
concentrations of dissolved salts reduces the availability of cadmium
to microorganisms and, therefore, reduces the toxic impact.
Freshwater microorganisms in culture are thus affected by cadmium at
lower concentrations than marine species (for example, 50 µg/litre
affects growth in many freshwater species of algae while at least 100
µg/litre, and often 1000 µg/litre, is required to reduce growth in
marine species). Soil microorganisms are partially protected from the
toxic effects of cadmium by the presence of clay.

5.1 Aquatic microorganisms

5.1.1 Freshwater microorganisms

Canton & Slooff (1982) exposed the bacterium Salmonella
typhimurium and the alga Chlorella vulgaris to cadmium in the form
of the chloride, and calculated an 8-h EC₅₀ (growth inhibition) of
10.4 mg/litre for the bacterium and a 96-h EC₅₀ of 3.7 mg/litre for
the alga. No-toxic-effect levels of 0.65 and 1.5 mg/litre were
estimated for the bacterium and alga, respectively. Jana &
Bhattacharya (1988) found significant inhibition of population growth
in the faecal coliform bacterium Escherichia coli during exposure to
cadmium concentrations of 1, 2 or 5 mg cadmium/litre for 7 or 28 days.
Cadmium was the most toxic of the metals tested. Norberg & Molin
(1983) exposed the bacterium Zoogloea ramigera (abundant in sewage
treatment plants) to cadmium chloride concentrations of 1, 3, 5, and
10 mg cadmium/litre for 30 h. A prolonged lag phase and decrease in
growth resulted, the length of the lag phase being proportional to the
concentration of cadmium in the medium. Babich & Stotzky (1977a)
showed that the presence of clay particles protected bacteria from the
toxic effect of cadmium added to culture medium. The degree of
protection was related to the cation exchange capacity of various
clays tested.

Chapman & Dunlop (1981) estimated the 8-h LC₅₀ for the
freshwater protozoan Tetrahymena pyriformis to be less than 1
mg/litre. However, this value increased with increasing water calcium
concentration; at a value of 500 mg calcium/litre, the LC₅₀ was 19
mg/litre. Magnesium also exerted a protective effect against cadmium
when mixed with calcium. Cadmium was consistently more toxic to
Tetrahymena in the presence of magnesium alone. Berk et al. (1985)
calculated a 15-min EC₅₀ (inhibition of ciliate chemotactic
response) for Tetrahymena sp. of 0.35-0.7 mg.

When Skowronski et al. (1988) exposed the green microalga
Stichococcus bacillaris to cadmium chloride concentrations of 45 and

90 µmol/litre for 4 days, growth rate was inhibited by 28% and 45% at
the two respective concentrations. At both exposure levels, dry weight
and chlorophyll a content were reduced in a dose-related manner.
Addition of manganese at concentrations of between 45 and 1800
µmol/litre had a dose-related antagonistic effect on cadmium toxicity.
Bennett (1990) found that the addition of cadmium (1.8 µmol/litre) to
a turbidostat culture of Chlorella pyrenoidosa caused a decrease in
the maximum specific growth rate (toxicity was expressed after a lag
of 5 generations). A gradual decrease in the maximum specific growth
rate was also noted during a 40-day exposure to stepwise increases in
the cadmium concentration (0.96 to 1.68 µmol/litre). The author found
that the addition of manganese (10.4 µmol/litre) had an antagonistic
effect, causing the maximum specific growth rate to increase.

Cadmium is toxic to the growth of the freshwater alga Chlorella
pyrenoidosa (Hart & Scaife, 1977). In cultures maintained at pH 7.0,
doubling times were 11, 21, 22, and 35 h for cadmium concentrations of
0, 0.25, 0.5, and 1.0 mg/litre medium, respectively. At a pH of 8.0,
the effect was somewhat lessened; doubling times were 11, 16, 17, and
25 h for the same range of cadmium doses. There was also a pronounced
effect on carbon dioxide fixation, which was reduced from 0.738 to
0.720, 0.558, and 0.283 µmol HCO₃^- fixed per hour with cadmium
exposures in the culture medium of 0, 0.246, 0.554, and 1.090
mg/litre, respectively. There was less of an effect on oxygen
evolution over the same dose range. Zinc offered no protection against
cadmium effects.

Wong et al. (1979) exposed four different species of freshwater
algae to cadmium and measured the uptake of ¹⁴C-carbonate.
Scenedesmus quadricaudata was the most sensitive species, carbonate
uptake being inhibited by 80% at a cadmium concentration of 20
µg/litre. Chlorella pyrenoidosa showed 70% inhibition of carbonate
uptake at about 100 µg/litre, while Chlorella vulgaris showed only
50% inhibition at about 500 µg/litre. The least sensitive of the four
species tested was Ankistrodesmus falcatus variety acicularis
where an effect on carbonate uptake started only at concentrations
higher than 500 µg/litre. There was no observed effect on the growth
of A. falcatus at cadmium concentrations lower than 5 mg/litre.
Rebhun & Ben-Amotz (1984) demonstrated that the chlorophyll content of
cells of Chlorella stigmatophora was reduced in a dose-dependant
manner across a range of cadmium concentrations of between 1 and 10
mg/litre medium.

Laegreid et al. (1983) studied the effects of cadmium on the alga
Selenastrum capricornutum cultured in the laboratory in water taken
from two lakes at various times throughout the year. The two lake
waters contained different amounts of organic material. The first
lake, a dystrophic bog lake, had a high organic content, while the
second, an eutrophic lake, had a low organic content. In the
dystrophic lake, which had a low pH (4.4), the toxicity of cadmium was
related to the free ionic concentration of the metal, as suggested by
many laboratory experiments. In the eutrophic lake, where there was

less influence from organic material, there was a pronounced seasonal
effect. In the summer, when growth and productivity of the algae were
highest, there was a much greater effect of the metal than predicted.
The toxicity of cadmium, at this time, was far greater than would be
expected even if all of the metal was in the free ionic form and none
was bound to organic compounds. On the basis of their field evidence,
the authors questioned the generally held assumption that organic
binding is the major factor in determining cadmium toxicity to
microorganisms. They considered that the presence of certain organic
compounds of low relative molecular mass could increase cadmium
toxicity. This conclusion is supported by the work of Giesy et al.
(1977), who found that uptake of cadmium into zooplankton could be
increased in the presence of organic compounds of low relative
molecular mass.

Chin & Sina (1978) investigated the cellular basis of cadmium
toxicity in microorganisms using cultures of Physarum polycephalum.
The organism was cultured, in plasmodial form, on the surface of
liquid medium, and replicate discs, cut from the protoplasmic sheet of
the organism, were used for the tests. The discs maintain mitotic
synchrony with each other and, therefore, cadmium could be introduced
at specific points in the cell cycle. The cultures were exposed to
cadmium sulfate (5 x 10^-4 mol/litre), which was floated onto the
surface of the culture medium. Exposure to cadmium immediately prior
to early prophase of mitosis extended the normal DNA replication
period from 3 h to 4 h; this was monitored using measurements of
uptake of ³H-thymidine. Two stages of the cell cycle were
particularly susceptible to cadmium. Exposure either at the beginning
of the cycle or 80% of the way through the cycle caused delays in the
completion of mitosis. A 30-min exposure to cadmium at the onset of
early prophase inhibited incorporation of ³H-uridine into RNA for
the following 3 h by 51% and stimulated the incorporation of
³H-thymidine into DNA, for the same period, by 85%. Later in the
cycle, DNA synthesis was inhibited and DNA content was depressed by
12.5%. There was an ultrastructural effect on the nucleoli (less dense
material centrally giving nucleoli in section a "ring" structure),
which was the only structural effect of the metal even after 4 h of
exposure. Accommodation occurred after pre-treatment with sub-