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    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)
                                                                                                                                   

    
    FIGURE 1

    FIGURE 2

    
    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         - 8d
                          mercury    9.1 d      - 49.7 d        8

                          zinc       1.9        -              -
    M2+-S2O32- 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

    FIGURE 3

    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.

    FIGURE 4

    
    Table 6.  Cadmium assimilation efficiencies in different soil invertebrates
                                                                                                                                    
                Species         Food              Cadmium concentration   Assimilation efficiency  Reference
                                                  in food (µmol/g)        (%)
                                                                                                                                    
    Snail
       Arianta arbusloruma       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-toxic
    doses of cadmium. Treatment with cadmium at the less sensitive periods
    of the cell cycle led to reduced effect at the more sensitive phases;
    the organism, in some way, compensated. There was no accommodation by
     Physarum after pre-treatment with zinc ions. This result contrasts
    with that of a similar study on  Escherichia coli where pre-exposure
    to zinc reduced the effects of cadmium (Mitra et al., 1975).

    5.1.2  Estuarine and marine microorganisms

         Chan & Dean (1988) exposed the marine bacterium  Pseudo-monas
     marina to cadmium sulfate at concentrations of 1 to 25 mg
    cadmium/litre. Effects were exposure related and included a lengthened
    lag time, reduced growth rate, reduced biomass and oxygen uptake, and
    a decrease in the activity of dehydrogenase and alkaline phosphatase.

    The IC50 values for inhibition of biomass and of growth rate were 11
    and 11.5 mg/litre, respectively. Flatau et al. (1987) progressively
    adapted the marine bacterium  Pseudomonas sp. to cadmium
    concentrations from 1 to 80 mg/litre. Although the length of the lag
    phase was not linearly or logarithmically correlated with the cadmium
    concentration, it was significantly longer at cadmium concentrations
    of 70 mg/litre or more. The growth rate was reduced at 10 mg/litre but
    remained constant at cadmium concentrations of 10 to 50 mg/litre; no
    growth was observed at 75 or 80 mg/litre. Oxygen consumption was not
    different from that of controls at 1 or 5 mg/litre but at
    concentrations of 10 mg/litre or more respiratory activity decreased.

         Bressan & Brunetti (1988) exposed the marine microalgae
     Dunaliella tertiolecta and  Isochrysis galbana to cadmium
    concentrations of 13.8 and 0.2 mg/litre, respectively, for up to 8
    days. Cadmium significantly reduced the population growth, expressed
    as the mean number of cells/ml, for both species. The addition of
    nitrilotriacetic acid (NTA, a sequestering agent) at ratios of 1:1,
    1:2 or 1:3 did not modify the toxic effect of cadmium.

         Berk et al. (1985) exposed the marine ciliates  Paranophrys sp.
    and  Miamiensis avidus to cadmium and monitored the inhibition of the
    chemotactic response. The 15-min EC50 values were 2-3.1 mg
    cadmium/litre and 5.1-7 mg cadmium/litre for the two species,
    respectively.

         Dongmann & Nurnberg (1982) investigated the effects of cadmium on
    the marine diatom  Thalassiosira rotula (a chain-forming diatom
    native to shallow temperate waters) in petri dish and in batch liquid
    cultures. They calculated generation times from the dish cultures and
    reported a toxicity threshold for generation time of 30 µmol
    cadmium/litre (3.4 mg/litre). At 50 µmol/litre, cadmium increased the
    generation time from 24 h to 28 h. Using chain length as a parameter,
    the toxicity threshold was 15 µmol/litre (1.7 mg/litre). Cell density
    was found to be affected in batch culture. Cell chlorophyll content
    and chain length were too variable to show significant effects of the
    metal in batch culture.

    5.2  Soil and litter microorganisms

         Babich & Stotzky (1977b) showed that several species of fungi
    tolerated cadmium to a greater degree when grown on cultures amended
    with clays than in pure culture medium.

         Sato et al. (1986) exposed the soil bacterium  Nitrosomonas
     europaea both to cadmium concentrations of 0.05, 0.1, and 0.4
    mg/litre and to a range of ammonia concentrations (1 to 100 mg/litre
    as N). Growth was markedly inhibited at the highest cadmium
    concentration, especially when this was coupled with ammonia
    concentrations greater than 10 mg/litre. Cadmium toxicity caused a
    characteristic growth response. Ammonia oxidation proceeded at a
    reduced rate for approximately 3 days and then fell sharply. The

    subsequent oxidation proceeded at a diminished but constant rate. At
    cadmium concentrations of 0.1 mg/litre or less, the toxic effect of
    cadmium could be partially offset by increasing the ammonia
    concentration. Prahalad & Seenayya (1988) found that cadmium
    concentrations of 3.5 mg/litre inhibited the growth of the bacterium
     Alcaligenes faecalis. However, if the nutrient broth was diluted by
    one half then growth was inhibited at 2 mg/litre, and with
    quarter-strength nutrient broth inhibition occurred at 0.5 mg/litre.

         Hartman (1974) reported less species diversity of soil fungi in
    areas of high cadmium contamination than in control areas. Samples of
     Fusarium oxysporium isolated from contaminated and control soils
    showed different tolerances to cadmium. This suggested the development
    of some resistance, presumably by selection of more resistant strains.

         Bond et al. (1976) incubated coniferous forest soil and litter
    (mixed with a pre-prepared homogeneous soil) in microcosm units and
    monitored oxygen consumption, carbon dioxide evolution, and bacterial
    and fungal populations. With cadmium added to a concentration of 0.01
    mg/kg soil and, in the initial stages of incubation, with cadmium at
    10 mg/kg soil, there was a stimulation of oxygen consumption,
    suggesting an effect of the metal on uncoupling of respiratory
    phosphorylation. In the later stages of incubation with cadmium at 10
    mg/kg there was a reduction in both oxygen consumption and carbon
    dioxide evolution. No effect was seen on numbers of organisms in the
    microcosms.

         Bewley & Stotzky (1983) investigated the effect of cadmium (100
    and 1000 mg/kg soil) on carbon mineralization and on the mycoflora in
    glucose-supplemented soils amended with clays (kaolinite or
    montmorillonite) at 9%. Cadmium had no significant effect on the
    length of the lag period, carbon dioxide evolution or on the amount of
    carbon mineralized. When subsequent cadmium additions of 2400 and 4000
    mg/kg were made to soils previously treated with 100 or 1000 mg/kg,
    the rate of glucose degradation decreased more in the clay-amended
    soils than in control soil not amended with clay. Clay protected fungi
    from the toxic effect of cadmium at 5000 mg/kg. Fungi from
    clay-treated soils were more sensitive to cadmium in the culture media
    after they had been isolated from soil pre-treated with cadmium. The
    authors interpreted these results as showing a reduction in the
    availability of cadmium to organisms in clay-amended soils. The
    overall effect would be a prevention of selection of more tolerant
    strains. Thus, when the organisms were challenged with high doses of
    cadmium, they would have been more susceptible than organisms from
    non-amended soil.

         Naidu & Reddy (1988) incubated black cotton soil (0.8% organic
    carbon; 55% clay) for up to 8 weeks in the presence of cadmium
    chloride at concentrations of between 50 and 500 mg cadmium/kg. The
    ammoniacal nitrogen (NH4-N) concentration increased for the first
    week at all treatment levels and then decreased at concentrations of
    50 mg/kg or less. The initial rise in NH4-N levels led to an

    increase in nitrate nitrogen (NO3-N) levels, the accumulation of
    NO3-N being inversely proportional to the cadmium exposure. The
    authors pointed out that at cadmium concentrations of 100 and 500
    mg/kg, hydrolysis of urea was significantly poorer than at other
    treatment levels, as shown by the lower concentration of NH4-N
    observed after 1 week. At all cadmium concentrations there was
    significant accumulation of nitrite nitrogen (NO2-N) at every sample
    time, compared to control soil, suggesting that cadmium might be toxic
    to soil nitrification. At all exposure levels cadmium significantly
    depressed both bacterial and fungal populations. Cadmium
    concentrations of 10 or 50 mg/kg had no effect on soil actinomycetes,
    but both 100 and 500 mg/kg significantly reduced the population. Tyler
    et al. (1974) incubated a mull soil for 7 weeks. Cadmium chloride
    concentrations of 9 to 18 µmol/g and cadmium acetate concentrations of
    9 to 22 µmol/g caused decreases in soil ammonium content and
    significantly increased nitrate accumulation.

    6.  TOXICITY TO AQUATIC ORGANISMS

    Appraisal

          Cadmium uptake from water by aquatic organisms is extremely
     variable and depends on the species and various environmental
     conditions such as water hardness (notably the calcium ion
     concentration), salinity, temperature, pH, and organic matter content
     (see chapter 4).

          The majority of chelating agents decrease cadmium uptake but
     some, such as dithiocarbamates and xanthates, increase uptake.

         As a consequence of the variability in cadmium uptake, the toxic
     impact to aquatic organisms also varies across a wide range of
     concentrations and is dependent on the species of organism and on the
     presence of other metal ions, notably calcium and zinc.

          The lowest recorded 96-h LC50 in a flow system is 16 µg
     cadmium per litre for the adult shrimp Mysidopsis bahia. A nominal
     no-observed-effect level (NOEL) of 0.6 µg cadmium/litre was found for
     Daphnia magna, reproductive rate being the most sensitive parameter.
     A nomi-nal NOEL has been noted at a similar level (1.7 to 3.4 µg
     cadmium per litre) with respect to the reproductive effects on brook
     trout.

          The available results indicate that the embryonic and larval
     stages of aquatic organisms are more sensitive than the adult stage.
     Spinal malformations are induced in cadmium-exposed fish. In addition
     to causing reproductive effects, cadmium influences the behaviour of
     aquatic organisms.

          At low concentrations, cadmium inhibits ion transport systems
     (10 µg cadmium/litre) and induces metallothionein synthesis (< 1 µg
     cadmium/litre) in freshwater fish.

    6.1  Toxicity to aquatic plants

         Hutchinson & Czyrska (1975) exposed two floating aquatic weeds,
    the common duckweed  Lemna minor and a floating fern  Salvinia
     natans, to cadmium concentrations of between 0.01 and 1.0 mg/litre
    for up to 3 weeks. Growth was reduced at all concentrations but
    especially at 0.05 mg/litre or more. The effect of cadmium on growth
    became more marked with time. Loss of green coloration (chlorosis) was
    a common symptom of cadmium toxicity, and at concentrations of 0.5 and
    1.0 mg/litre  Lemna plants died. When the two species were grown in
    competition, growth at lower cadmium concentrations (0.01 and 0.05
    mg/litre) was greater in  Salvinia but less in  Lemna than when the
    plants were grown alone.

         In a study by Nir et al. (1990), water hyacinth plants were
    exposed to cadmium concentrations of 0, 0.05, 0.1, 0.4 or 1.0 mg/litre

    for 7 days. Concentrations of 0.1 mg/litre or less had no significant
    effect on wet or dry biomass gain or on chlorophyll  a content.
    Concentrations of 0.4 or 1.0 mg/litre significantly reduced both wet
    biomass gain and chlorophyll  a content but had no significant effect
    on dry biomass gain. The chlorophyll  a content of leaves decreased
    with time in plants exposed to 0.4 mg/litre. After 3 weeks of
    exposure, the chlorophyll  a levels were 75% lower than in control
    plants.

    6.2  Toxicity to aquatic invertebrates

         Cadmium is moderately to highly toxic to aquatic invertebrates
    (see Tables 9 and 10). Its toxic effect is dependent on a variety of
    environmental variables. Factors that reduce the free ionic
    concentration, e.g., water hardness, salinity, chelating agents, and
    high organic content of water, tend to reduce the toxic effect of
    cadmium. The presence of zinc increases the toxic effect of cadmium on
    invertebrates.

    6.2.1  Acute and short-term toxicity

         The acute toxicity of cadmium to aquatic invertebrates, as
    assessed in laboratory tests, is summarized in Tables 9 and 10. The
    most notable features are the variability in cadmium toxicity between
    different organisms and the effects of temperature, salinity, and
    water hardness. There is considerable variation even amongst closely
    related species.

         In a study by Canton & Slooff (1982), the water flea  Daphnia
     magna was exposed to cadmium over a 48-h period. At a water hardness
    of 1 mmol/litre there was no mortality at 16 µg cadmium per litre,
    while at a water hardness of 2 mmol/litre there was no mortality or
    abnormal behaviour at 17 µg/litre.

         Clubb et al. (1975b) investigated the toxicity of cadmium to nine
    species of aquatic insects, but seven of the species tested were too
    insensitive to the effects of the metal for the LC50 to be
    determined. The insensitive species were  Atherix variegata,
     Hexatoma sp.,  Holorusia sp.,  Acroneuria pacifica,  Arcynopteryx
     signata,  Pteronarcys californica, and  Brachycentrus americanus;
    these species represented Dipterans (true flies), Plecoptera
    (stoneflies), and Tricoptera (caddis flies).

    
    Table 9.  Toxicity of cadmium to marine or estuarine invertebrates
                                                                                                                                    
    Organism             Size/      Stat/ Temperature  Salinity  pH       Duration  LC50                    Reference
                         age        flow a     (°C)     (%)                (h)       (mg/litre)b
                                                                                                                                    
    Purple sea urchin    embryo     stat  8.2-8.4      30        7.8-8.1  120       0.5 (0.4-0.6) m         Dinnel et al. (1989)
      (Strongylocentrotus
       purpuratus)

    Green sea urchin     embryo     stat  8.2-8.4      30        7.8-8.1  120       1.8 (1.5-2.2) m         Dinnel et al. (1989)
      (Strongylocentrotus
       droebachiensis)

    Sand dollar          embryo     stat  12.5-13.0    30        8.0-8.1  72        7.4 (5.2-10.8) m        Dinnel et al. (1989)
      (Dendraster
       excentricus)

    Starfish             24.5 g     stat  20           20        8.0      24        12 n                    Eisler (1971)
      (Asterias forbesi) 24.5 g     stat  20           20        8.0      48        1.0 n                   Eisler (1971)
                         24.5 g     stat  20           20        8.0      96        0.82 n                  Eisler (1971)
                         11.2 g     stat  20           20        7.8      24        71 n                    Eisler & Hennekey (1977)
                         11.2 g     stat  20           20        7.8      48        7.1 n                   Eisler & Hennekey (1977)
                         11.2 g     stat  20           20        7.8      96        0.7 n                   Eisler & Hennekey (1977)

    American oyster      embryo     stat  26           25        7.0-8.5  48        3.8 (2.85-4.48) n       Calabrese et al. (1973)
      (Crassostrea
       virginica)

    Mussel                          stat  18.5         32.9      7.9      96        1.62 (1.19-2.22) m      Ahsanullah (1976)
      (Mytilus edulis
       planulatis)

    Blue mussel          4 g        stat  20                     8.0      24        > 200 n                 Eisler (1971)
      (Mytilus edulis)   4 g        stat  20                     8.0      48        165 n                   Eisler (1971)
                         4 g        stat  20                     8.0      96        25 n                    Eisler (1971)

    Table 9 (contd).
                                                                                                                                    
    Organism             Size/      Stat/ Temperature  Salinity  pH       Duration  LC50                    Reference
                         age        flow a     (°C)     (%)                (h)       (mg/litre)b
                                                                                                                                    
    Soft-shell clam      5.2 g      stat  20           20        8.0      24        > 20 n                  Eisler (1971)
      (Mya arenaria)     5.2 g      stat  20           20        8.0      48        50 n                    Eisler (1971)
                         5.2 g      stat  20           20        8.0      96        2.2 n                   Eisler (1971)
                         4.6 g      stat  20           20        7.8      24        32 n                    Eisler & Hennekey (1977)
                         4.6 g      stat  20           20        7.8      48        2.5 n                   Eisler & Hennekey (1977)
                         4.6 g      stat  20           20        7.8      96        0.7 n                   Eisler & Hennekey (1977)

    Bay scallop          20-30 mm   stat  20           25        8.0      24        8.2 n                   Nelson et al. (1976)
      (Argopecten        20-30 mm   stat  20           25        8.0      48        3.21 n                  Nelson et al. (1976)
       irradians)        20-30 mm   stat  20           25        8.0      72        2.18 n                  Nelson et al. (1976)
                         20-30 mm   stat  20           25        8.0      96        1.48 (0.95-2.31) n      Nelson et al. (1976)

    Atlantic oyster      0.6 g      stat  20           20        8.0      24        158 n                   Eisler (1971)
    drill                0.6 g      stat  20           20        8.0      48        28 n                    Eisler (1971)
      (Urosalpinx        0.6 g      stat  20           20        8.0      96        6.6 n                   Eisler (1971)
       cinerea)

    Eastern mud snail    0.56 g     stat  20           20        8.0      24        > 200 n                 Eisler (1971)
      (Nassarius         0.56 g     stat  20           20        8.0      48        125 n                   Eisler (1971)
       absoletus)        0.56 g     stat  20           20        8.0      96        10.5 n                  Eisler (1971)

    Ragworm              8 g        stat  20           20        8.0      24        25 n                    Eisler (1971)
      (Nereis virens)    8 g        stat  20           20        8.0      48        25 n                    Eisler (1971)
                         8 g        stat  20           20        8.0      96        11 n                    Eisler (1971)
                         7.6 g      stat  20           20        7.8      24        56 n                    Eisler & Hennekey (1977)
                         7.6 g      stat  20           20        7.8      48        9.3 n                   Eisler & Hennekey (1977)
                         7.6 g      stat  20           20        7.8      96        0.7 n                   Eisler & Hennekey (1977)

    Copepod              nauplius   stat  22           10                 96        0.06 (0.001-0.2) m      Roberts et al. (1982)
      (Eurytemora affinis)

    Copepod              adult      stat  22           10                 96        0.38 (0.006-1.52) m     Roberts et al. (1976)
      (Acartia tonsa)

    Table 9 (contd).
                                                                                                                                    
    Organism             Size/      Stat/ Temperature  Salinity  pH       Duration  LC50                    Reference
                         age        flow a     (°C)     (%)                (h)       (mg/litre)b
                                                                                                                                    
    Harpacticoid
      copepod            adult      stat  20-22        3                  96        0.43 (0.31-0.55)        Bengtsson & Bergstrom (1987)
      (Nitocra spinipes) adult      stat  20-22        7                  96        0.66 (0.53-0.82)        Bengtsson & Bergstrom (1987)
                         adult      stat  20-22        15                 96        0.78 (0.41-120)         Bengtsson & Bergstrom (1987)

    Marine amphipod      young      stat  10                              96        3.5 m                   Wright & Frain (1981a)
      (Marinogammarus    adult      stat  10                              96        13.3 m                  Wright & Frain (1981a)
       obtusatus)

    Mysid shrimp         adult      flow  22           20        7.3      96        0.036 (0.022-0.081) m   Roberts et al. (1982)
      (Neomysis          adult      flow  22           20        7.8      96        0.02 (0.015-0.027) m    Roberts et al. (1982)
       americanus)

    Mysid shrimp         adult      stat  22           20        7.3      96        0.017 m                 Roberts et al. (1982)
      (Mysidopsis bahia) adult      stat  22           20        7.7      96        0.029 (0.013-0.043) m   Roberts et al. (1982)
                                    flow c20-28        15-23              96        0.016 (0.013-0.02) m    Nimmo et al. (1978)

    Shrimp                          stat  18.7         32.1      8.0      120       2.3 (1.05-5.06) m       Ahsanullah (1976)
      (Palaemonetes sp.)            stat  18.7         32.1      8.0      168       1.85 (1.32-2.59) m      Ahsanullah (1976)
                         0.38 g     flow  16.8                            96        6.8 (5.2-9.76) m        Ahsanullah (1976)
                         0.16 g     flow  17.8                   8.1      96        6.4 (5.73-7.19) m       Ahsanullah (1976)

    Sandworm             0.37 g     stat  18.5         32.7      8.1      168       6.4 (5.82-7.1) m        Ahsanullah (1976)
      (Neanthes vaali)

    Sand shrimp          0.25 g     stat  20           20        8.0      24        2.4 n                   Eisler (1971)
      (Crangon           0.25 g     stat  20           20        8.0      48        0.5 n                   Eisler (1971)
       septemspinosa)    0.25 g     stat  20           20        8.0      96        0.32 n                  Eisler (1971)

    Sand shrimp          adult      flow  10.2         28.6      7.9      96        2.3 (1.7-5.1) m         Dinnel et al. (1989)
      (Crangon spp.)

    Table 9 (contd).
                                                                                                                                    
    Organism             Size/      Stat/ Temperature  Salinity  pH       Duration  LC50                    Reference
                         age        flow a     (°C)     (%)                (h)       (mg/litre)b
                                                                                                                                    
    Grass shrimp         0.33 g     stat  20           20        8.0      24        43 n                    Eisler (1971)
      (Palaemonetes      0.33 g     stat  20           20        8.0      48        3.7 n                   Eisler (1971)
       vulgaris)         0.33 g     stat  20           20        8.0      96        0.32 n                  Eisler (1971)

    Shrimp                          stat               35                 96        2.07 (± 0.22) m         McClurg (1984)
      (Penaeus indicus)

    Pink shrimp                     flow  25           20                 96        4.6 m                   Bahner & Nimmo (1975)
      (Penaeus duorarum)

    Grapsid crab         1.47 g     stat  17.8         32.6      8.1      168       14 (11.2-17.5) m        Ahsanullah (1976)
      (Paragrapsus       1.08 g     stat  17.1                            168       16.7 (15.11-18.45)      Ahsanullah (1976)
       quadridentatus)

    Hermit crab          0.47 g     stat  20           20        8.0      24        > 200 n                 Eisler (1971)
      (Pagurus           0.47 g     stat  20           20        8.0      48        3.7 n                   Eisler (1971)
       longicarpus)      0.47 g     stat  20           20        8.0      96        0.32 n                  Eisler (1971)
                         0.5 g      stat  20           20        7.8      24        15 n                    Eisler & Hennekey (1977)
                         0.5 g      stat  20           20        8.0      96        1.3 n                   Eisler & Hennekey (1977)

    Shore crab           5.9 g      stat  20           20        8.0      24        100 n                   Eisler (1971)
      (Carcinus maenus)  5.9 g      stat  20           20        8.0      48        16.6 n                  Eisler (1971)
                         5.9 g      stat  20           20        8.0      96        4.1 n                   Eisler (1971)

    Dungeness crab       zoea       stat  8.5          30        8.1      96        0.2 (0.1-0.4) m         Dinnel et al. (1989)
      (Cancer magister)

    Squid                larva      stat  8.6          30        8.1      96        > 10.2 m                Dinnel et al. (1989)
      (Loligo opalescens)
                                                                                                                                    

     a stat = static conditions (water unchanged for duration of test); flow = flow-through conditions (cadmium concentration
       in water continuously maintained) unless stated otherwise
     b organisms exposed to cadmium added as cadmium chloride; m = measured; n = nominal
     c intermittent flow-through conditions

    Table 10.  Toxicity of cadmium to freshwater invertebrates
                                                                                                                                    

    Organism               Size/      Stat/  Temperature  Hardness c  pH       Duration LC50d                  Reference
                           age        flow a   (°C)         (mg/litre)         (h)      (mg/litre)
                                                                                                                                    
    Snail                  adult      stat   20-22                    6.7      24       7.6 n                  Wier & Walter (1976)
      (Physa               adult      stat   20-22                    6.7      48       4.25 n                 Wier & Walter (1976)
       gyrina)             adult      stat   20-22                    6.7      96       1.37 n                 Wier & Walter (1976)
                           adult      stat   20-22                    6.7      228      0.83 n                 Wier & Walter (1976)
                           immature   stat   20-22                    6.7      48       0.69 n                 Wier & Walter (1976)
                           immature   stat   20-22                    6.7      96       0.41 n                 Wier & Walter (1976)

    Snail                             flow b  15                      7.1-7.7  168      0.114 m                Spehar et al. (1978a)
      (Physa integra)

    Snail                  10-12 mm   flow   12           128-176     7.7      24       4.4 m                  Williams et al. (1985)
      (Physa               10-12 mm   flow   12           128-176     7.7      48       2.1 m                  Williams et al. (1985)
       fontinalis)         10-12 mm   flow   12           128-176     7.7      96       0.8 m                  Williams et al. (1985)

    Isopod                 8-10 mm    flow   12           128-176     7.7      24       13 m                   Williams et al. (1985)
      (Asellus             8-10 mm    flow   12           128-176     7.7      48       3.6 m                  Williams et al. (1985)
       aquaticus)          8-10 mm    flow   12           128-176     7.7      96       0.6 m                  Williams et al. (1985)

    Scud                                     10                                96       0.12 m                 Wright & Frain (1981b)
      (Gammarus            8-12 mm    flow   12           128-176     7.7      24       1.6 m                  Williams et al. (1985)
       pulex)              8-12 mm    flow   12           128-176     7.7      48       0.4 m                  Williams et al. (1985)
                           8-12 mm    flow   12           128-176     7.7      96       0.02 m                 Williams et al. (1985)

    Water flea             adult      stat   10           0.85 meq/   7.2      48       0.055 e (0.032-0.095) n Baudouin & Scoppa (1974)
      (Daphnia hyalina)                                     litre

    Water flea             1 day      stat   20           7.6-7.7     24       3 n      Kuhn et al. (1989)
      (Daphnia             < 1 day    stat   20-22        110-130     7.8      48       0.04 (0.02-0.07) n     Hall et al. (1986)
       magna)              < 1 day    stat   20-22        190-210     7.7      48       0.08 (0.06-0.1) n      Hall et al. (1986)
                           < 1 day    stat   18-20        1 mmol/              48       0.03 m                 Canton & Slooff (1982)
                                                          litre

    Table 10 (contd).
                                                                                                                                    

    Organism               Size/      Stat/  Temperature  Hardness c  pH       Duration LC50d                  Reference
                           age        flow a   (°C)         (mg/litre)         (h)      (mg/litre)
                                                                                                                                    
    Water flea             < 1 day    stat   20-22        110-130     7.8      48       0.07 n                 Hall et al. (1986)
      (Daphnia             < 1 day    stat   20-22        110-130     7.7      48       0.1 (0.07-0.12) n      Hall et al. (1986)
       ulex)               < 1 day    stat   19-22                    7.7      96       0.047 (0.042-0.052) n  Bertram & Hart (1979)

    Copepod                adult      stat   10           0.85 meq/   7.2      48       3.8 e (2.3-6.3) n       Baudouin & Scoppa (1974)
      (Cyclops abyssorum)                                   litre

    Copepod                adult      stat   10           0.85 meq/   7.2      48       0.55 e (0.39-0.77) n    Baudouin & Scoppa (1974)
      (Eudiaptomus padanus)                                 litre

    Crayfish                          flow   19-21        24-28      6.7-7.0    96      6.1 (4.7-7.9) m        Mirenda (1986)
      (Orconectes virilis)

    Mayfly                            flow   10                        7.8      96      28 m                   Clubb et al. (1975b)
      (Ephemerella grandis
       grandis)

    Midge                  10-12 mm   flow   12           128-176     7.7      96       300 m                  Williams et al. (1985)
      (Chironomus riparius)

    Stonefly                          flow   10                       7.8      96       18 m                   Clubb et al. (1975b)
      (Pteronarcella badia)

    Stonefly               10-15 mm   flow   12           128-176     7.7      96       520 m                  Williams et al. (1985)
      (Hydropsyche
       angustipennis)
                                                                                                                                    

     a stat = static conditions (water unchanged for duration of test); flow = flow-through conditions (cadmium concentration
       in water continuously maintained) unless stated otherwise
     b intermittent flow-through conditions
     c hardness expressed as mg CaCO3/litre unless stated otherwise
     d organisms exposed to cadmium added as cadmium chloride unless otherwise stated; m = measured concentration; n = nominal concentration
     e organism exposed to cadmium as cadmium sulfate

    
         Spehar et al. (1978a) reported a decreased survival of the water
    snail  Physa integra at a cadmium concentration of 85.5 µg/litre
    after 7 days of exposure. After 21 days of exposure, survival was
    significantly decreased at 27.5 µg/litre, the next lowest
    concentration tested. Some snails exposed to these concentrations
    developed a condition in which the animal was extended from the shell
    but unable to attach the foot or crawl. A white mucus layer covered
    the exposed foot region of some snails and these subsequently died.
    Concentrations tested were not high enough to obtain a 4-day LC50
    value but the 7-day LC50 of 114 µg/litre was approximately 11 times
    higher than the 28-day LC50 value of 10.4 µg/litre.

         Mirenda (1986) reported a 14-day LC50 of 0.7 mg cadmium per
    litre for the crayfish  Orconectes virilis under flow-through
    conditions. Pesch & Stewart (1980) estimated the 10-day LC50 for bay
    scallops  Argopecten irradians to be 0.53 mg/litre in flowing sea
    water. The EC50 (for growth) for the same species over 42 days was
    0.078 mg/litre. Byssal thread detachment, which precedes death, showed
    an EC50 of 0.54 mg/litre of cadmium 8 days into the test and before
    there was any appreciable mortality. Robinson et al. (1988) compared
    10-day LC50 values for freshly collected and cultured infaunal
    amphipods ( Rhepoxynius abronius). Cultured amphipods appeared normal
    and survived well (93%) under control toxicity test conditions, but
    were more sensitive to cadmium in sediment (10-day LC50 = 4.4 mg/kg)
    than were freshly caught amphipods (10-day LC50 = 8.7 mg/kg).

         When Winner (1988) exposed  Daphnia magna and  Ceriodaphnia
     dubia to cadmium for 7 days, the most sensitive indicators were mean
    body length of primiparous females in  D. magna, which was
    significantly reduced at 2 µg cadmium/litre, and the total young per
    female in  C. dubia, significantly reduced at 1 µg/litre.

    6.2.1.1  Effects of temperature and salinity on acute toxicity

         An increase in toxicity as temperature increases and as salinity
    decreases is valid for all organisms that have been tested with these
    variables (Tables 9 and 10).

         O'Hara (1973) investigated the effects of temperature and
    salinity on the toxicity of cadmium to adult male and female fiddler
    crabs ( Uca pugilator). Mortality was greatest at high temperatures
    and low salinities in tests lasting 240 h. LC50 values varied from
    2.9 mg/litre for the lowest salinity (10%) and highest temperature (30
    °C) to 47.0 mg/litre for the highest salinity (30%) and lowest
    temperature (10 °C). Frank & Robertson (1979) exposed the blue crab
    ( Callinectes sapidus) to cadmium chloride at salinities of 1, 15,
    and 35%. Like O'Hara, they found a decrease in cadmium toxicity with
    increase in salinity. For example, 96-h LC50 values were 0.32, 4.7,
    and 11.6 mg cadmium/litre for the three salinities, respectively.
    Rosenberg & Costlow (1976) reported increased cadmium toxicity during
    larval development of two estuarine crab species as salinity decreased
    and increased toxicity as temperature increased.

         Voyer & Modica (1990) found the same pattern with the mysid
    shrimp  Mysidopsis bahia. For salinities of 10 and 30%, the 96-h
    LC50 values ranged from 15.5 to 28 µg cadmium/litre at a temperature
    of 25 °C and from 47 to 84 µg/litre at a temperature of 20 °C. At 30
    °C the 96-h LC50 was < 11 µg/litre at both salinities. However,
    when Robert & His (1985) exposed embryos and larvae of the Japanese
    oyster  Crassostrea gigas to cadmium concentrations of up to 50
    µg/litre at various salinities (20 to 35%), decreasing the salinity
    severely affected the development of the oysters but cadmium had no
    effect.

         At temperatures higher than 11 °C, the combined effect of
    temperature and cadmium caused a heavy stress to the copepod  Tisbe
     holothuriae so that the effects of salinity were masked
    (Verriopoulos & Moraitou-Apostolopoulou, 1981).

    6.2.1.2  Effect of water hardness

         Using either artificial hard water (hardness: 180 mg CaCO3 per
    litre) or dechlorinated tap water (hardness: 60 mg/litre),
    Niederlehner et al. (1984) conducted short-term tests on the effects
    of cadmium on the freshwater oligochaete  Aeolosoma headlyi.
    Mortality and population growth/maintenance were assessed over 10 to
    14 days. The authors established NOEL values for population growth of
    32.0 and 53.6 µg/litre for hard water (two replicate tests), whereas
    the NOEL for the softer water was 17.2 µg/litre. The 48-h LC50
    values were 4.98 and 1.2 mg/litre, respectively, for hard and softer
    water.

    6.2.1.3  Effect of organic materials and sediment

         When Schuytema et al. (1984) exposed  Daphnia magna to cadmium
    for a period of 48 h, the mean LC50 value was 39 µg/litre in water
    and 91 µg/litre in a water-sediment slurry. Giesy et al. (1977) found
    that cadmium was more toxic to water fleas ( Simocephalus serrulatus)
    exposed in well water with a low organic content than to those exposed
    in pond water with a high organic content. The authors isolated a
    series of organic fractions from the pond water by ultrafiltration.
    Protection against cadmium toxicity was afforded by fractions of
    intermediate relative molecular mass (ranging from approximately 500
    to 300 000 daltons). The fraction with a relative molecular mass in
    excess of 300 000 daltons marginally increased the toxicity of
    cadmium.

         Kemp & Swartz (1988) compared the acute toxicity of interstitial
    and particle-bound cadmium to the marine infaunal amphipod
     Rhepoxynius abronius. The cadmium concentration in interstitial
    water was kept constant whereas the sediment cadmium level was varied
    by using perfusion through the sediment with peristaltic pumps. The
    principal cause of toxicity was found to be cadmium dissolved in
    interstitial water, between 70 and 88% of the toxicity being
    predictable from interstitial water concentrations.

    6.2.1.4  Lifestage sensitivity

         When Calabrese et al. (1973) investigated the toxicity of cadmium
    to embryos of the American oyster  Crassostrea virginica, there was
    no mortality at 1 mg/litre and the 48-h LC50 and LC100 values were
    3.8 and 6 mg/litre, respectively. Johnson & Gentile (1979) found the
    larva of the American lobster  Hommarus americanus to be sensitive to
    cadmium; the 96-h LC50 in static bioassays was 78 µg/litre. The
    mortalities after 96 h at concentrations of 10 and 30 µg/litre were 3%
    and 10%, respectively. There is a very steep increase in toxicity of
    cadmium to lobster larvae between 24 and 96 h. The 24-h LC50 is
    approximately 1 mg/litre; at this concentration the mortality reaches
    100% within 48 h.

         Verriopoulos & Moraitou-Apostolopoulou (1982) found that the
    different life-stages of the copepod  Tisbe holothuriae showed
    differences in sensitivity to cadmium. One-day-old nauplius larvae of
    the copepod were the most sensitive with an LC50 of 0.538 mg/litre,
    expressed as ions of cadmium, while 5-day-old nauplii showed an LC50
    of 0.645 mg/litre. The value for 10-day-old copepodids (0.906
    mg/litre) was not significantly different from that for adult females
    (0.916 mg/litre). Females with ovigerous sacs were slightly more
    sensitive, with an LC50 of 0.873 mg/litre. When Robinson et al.
    (1988) exposed the infaunal phoxocephalid amphipod  Rhepoxynius
     abronius to sediment contaminated with cadmium, the 10-day LC50
    values were 8.2 mg/kg for juveniles and 11.5 mg/kg for adults.

         Nebeker et al. (1986) exposed  Daphnia magna of different ages
    to cadmium for a period of 48 h. Mean EC50 (immobilization) values
    ranged from 23 µg/litre for 6 day-old water fleas to 164 µg/litre for
    2-day-old  Daphnia. Tests on  Daphnia of different ages, conducted
    in water of different hardness (32 or 76 mg CaCO3 per litre), with
    or without feeding and in two different sizes of container, resulted
    in a wide range of EC50 values (4 to 307 µg/litre). There was no
    consistent effect of any of these variables other than the age of the
    test animals. Very young animals were relatively tolerant, with a mean
    EC50 value of 109 µg/litre.

         McCahon et al. (1989) exposed both cased and uncased 1st, 3rd,
    and 4th larval instars of the caddis fly  Agapetus fuscipes to
    cadmium chloride. The LC50 values ranged from 295 to > 1000 mg
    cadmium/litre at 24 h and from 50 to 320 mg/litre at 96 h. First
    instar larvae were significantly more sensitive than 3rd or 4th instar
    larvae and at all ages cased animals were more resistant than uncased.

    6.2.1.5  Other factors affecting acute and short-term toxicity

         Chandini (1988; 1989) found that increasing the food source of
    the cladocerans  Daphnia carinata and  Echinisca triserialis greatly
    reduced the toxicity of cadmium, expressed as the 48-h or 96-h LC50,
    and the effect of cadmium on various other life history parameters,
    such as fecundity, growth, and age at first reproduction.

         Verriopoulos & Moraitou-Apostolopoulou (1981) exposed adult
    females of the copepod  Tisbe holothuriae to cadmium and found that
    the oxygen concentration in the water was negatively related to
    mortality and that population density was positively related after
    cadmium exposure. Clubb et al. (1975a) showed that the toxicity of
    cadmium to aquatic insects decreased with decreasing dissolved oxygen
    levels in the test water.

         McCahon et al. (1988) exposed the amphipod  Gammarus pulex to
    cadmium chloride under static conditions and reported a 96-h LC50 of
    0.05 mg cadmium/litre. The acute toxicity of cadmium to  G. pulex
    parasitized by the acanthocephalan  Pomphorhynchus laevis at several
    levels of infection was investigated. Toxicity, expressed as LC50,
    did not differ significantly between uninfected and infected
    amphipods.

         Kay & Haller (1986) fed water hyacinth weevils  Neochetina
     eichhorniae on water hyacinths containing cadmium from previous
    exposure to the metal. There was no mortality in weevils fed on leaves
    containing up to 17.2 mg cadmium/kg. At this exposure level, the
    weevils accumulated a cadmium body burden of 36.67 mg/kg over 20 days.

    6.2.2  Long-term toxicity

         In a study by Zaroogian & Morrison (1981), adult and larval
    oysters of the species  Crassostrea virginica were exposed to cadmium
    at concentrations of 5 or 15 µg/litre. Some adults were exposed (for
    35 or 37 weeks) to cadmium at these two concentrations prior to
    spawning, and larvae from these pre-treated adults and from control
    treated adults were reared in either control sea water or sea water
    containing 5 or 15 µg/litre cadmium. In all there were 11 treatment
    combinations. The highest larval mortality occurred when larvae from
    parents treated with 15 µg/litre were reared in sea water containing
    15 µg/litre for 3 weeks. However, larvae that survived this treatment
    grew to lengths not significantly different from controls. The effects
    observed with other treatment combinations were only temporary. Growth
    and development were slowed but those larvae that survived ultimately
    developed normally and to the same size as controls.

         When Holcombe et al. (1984) exposed snails, from embryos through
    to adult sexual maturity, to cadmium chloride, there was a delayed
    hatch, a reduction in percentage hatch and survival, and reduced
    growth when compared to controls. Based on these effects, the authors
    suggested a maximum acceptable cadmium concentration in water of
    between 4 and 8 µg/litre from one test and between 2 and 5 µg/litre
    from a replicate test.

         Lussier et al. (1985) conducted life-cycle tests, over 35 days,
    on the mysid shrimp  Mysidopsis bahia. Cadmium affected survival
    primarily and no reproductive effects were noted at sublethal
    concentrations.

         Following a long-term investigation in the laboratory and in the
    field, Marshall (1979) suggested a chronic LC10 for the water flea
     Daphnia galeata mendotae of 0.15 µg cadmium/litre. Winner (1986)
    exposed  Daphnia pulex chronically (21 or 42 days) to cadmium, added
    as cadmium sulfate, under different water conditions. Increasing the
    water hardness from 58 to 116 mg/litre reduced the toxic effect of the
    cadmium but a further increase to 230 mg/litre had no further effect.
    The most sensitive aspect of the  Daphnia life history to cadmium was
    the abortion rate of young. Humic acid had no effect on this parameter
    in soft or medium-hard water but increased the toxic effect of cadmium
    in hard water. Mortality was increased by humic acid (0.75 or 1.50
    mg/litre) at all water hardness levels. van Leeuwen et al. (1985)
    calculated 14-day and 21-day LC50S for  Daphnia magna of 24 and 14
    µg cadmium/litre, respectively. No effect on mortality was seen at 3.2
    µg/litre. The lowest concentrations producing significant mortality of
    young amphipods during 6-week exposures to cadmium were 1 µg/litre for
     Hyalella azteca and 3.2 µg/litre for  Gammarus fasciatus (Borgmann
    et al., 1989b).

    6.2.3  Reproductive effects

         Mysing-Gubala & Poirrier (1981) conducted laboratory experiments
    on the effect of cadmium on the freshwater sponge  Ephydatia
     fluviatilis. Sponge cuttings were exposed to cadmium concentrations
    ranging from 0.001 to 1.0 mg/litre for 1 month. At the end of the
    experimental period, the cuttings were classified in four groups
    depending on whether the sponge survived, whether it produced asexual
    reproductive gemmules, and whether the silicaceous spicules of the
    gemmules were normal or malformed. There was some effect of cadmium
    even at concentrations as low as 0.001 mg/litre, 17% of the sponge
    cuttings showing no gemmule production and 33% showing malformed
    spicules. At concentrations of 0.5 and 1.0 mg/litre, all of the sponge
    cuttings died.

         Lee & Xu (1984) investigated the effects of cadmium at 0.5 and
    0.1 mg/litre on the fertilization and development of sea urchin eggs
    and the development of  Amphioxus. At both cadmium concentrations,
    sea urchin development was normal to the gastrulation stage but all
    the plutei were abnormal. The effects on  Amphioxus development were
    different; cleavage of eggs was not affected by cadmium at 0.5 or 0.1
    mg/litre but neurulation was. Dinnel et al. (1989) exposed sperm from
    various sea urchin species to cadmium chloride for 60 min and assessed
    fertilization success; EC50 values ranged from 12 to 26 mg/litre. An
    EC50 of 8 mg/litre was calculated for the sand dollar  Dendraster
     excentricus. Den Besten et al. (1989) exposed the sea star  Asterias
     rubens to cadmium chloride at a concentration of 25 µg cadmium/litre
    for 5 months. No effect on spermatozoa was found, but maturation of
    oocytes was delayed and early development of embryos was adversely
    affected.

         Conrad (1988) studied the effect of cadmium on newly fertilized
    eggs of the mud snail  Ilyanassa obsoleta. No apparent effect was

    observed at a cadmium concentration of 10-6 mol/litre. The minimum
    concentrations producing abnormal veliger development and abnormal
    late cleavage and stopping early cleavage were 10-5-10-4
    mol/litre, 10-3 mol/litre, and 10-3 mol/litre, respectively.

         Biesinger & Christensen (1972) estimated a 3-week 16%
    reproductive impairment concentration of 0.17 µg cadmium/litre.

         In a 21-day reproduction test on  Daphnia magna, Kuhn et al.
    (1989) determined a nominal NOEL of 0.6 µg Cd2+/litre, reproduction
    rate being the most sensitive parameter. A nominal NOEL of 1 µg/litre
    was found when daphnids were exposed to the cadmium chloride salt.
    Reproduction of  Daphnia magna was completely inhibited at
    concentrations exceeding 3.2 µg/litre and time-dependant survival and
    reproduction were significantly reduced at 1.8 µg/litre. No effects on
    reproduction were observed at 1 µg/litre (van Leeuwen et al., 1985).
    When Bertram & Hart (1979) exposed the cladoceran  Daphnia pulex to
    cadmium concentrations of 1 to 30 µg/litre, there was no significant
    effect on the number of days required for onset of reproduction or on
    its frequency. At 1 µg/litre no significant effect on longevity of
    individuals was observed, but at concentrations of 5 µg/litre or more
    there was a significant reduction. All cadmium concentrations caused
    a reduction in the average brood size, the average number of broods
    per adult, and the total number of progeny. The authors also exposed
    daphnids to cadmium-contaminated food in the form of the phytoplankton
     Chlorella, the cadmium concentration being 0.3-0.6 µg cadmium/litre
    of medium. This resulted in a significant reduction in the average
    number of broods per adult and the average brood size. However, there
    was no significant effect on average longevity of individuals, the
    percentage of adults producing broods, the average number of days to
    the first brood or the average number of days between broods.

         Bengtsson & Bergstrom (1987) exposed newly fertilized female
    harpacticoids ( Nitocra spinipes) to cadmium chloride at two
    salinities for 13 days. At 3% the fecundity EC50 was 37-46 µg/litre
    at a salinity of 3% and 6-15 µg/litre at 15%.

         Williams et al. (1987) provided water containing nominal cadmium
    chloride concentrations of 0, 0.3, 30, 100 or 300 mg cadmium/litre
    cadmium to newly-emerged adults of the midge  Chironomus riparius in
    which they could lay their eggs. The females preferred to lay their
    eggs in water with no cadmium or in the lower concentrations;
    significant preferences were recorded. Eggs of Chironomids are laid
    within a protective gelatinous matrix. Eggs exposed to cadmium after
    complete formation of the matrix in control water were unaffected (the
    hatch was 80-100%), whereas those exposed after removal of the matrix
    had a reduced hatching rate (60%) at all test concentrations. Eggs
    laid directly in water containing cadmium were unaffected by a
    concentration of 0.3 mg/litre, but hatching rates were reduced to 45%
    at 30 mg/litre, 8% at 100 mg/litre, and 0% at 300 mg/litre. Clearly,
    cadmium only affects the unprotected egg, either when it is newly laid

    and before its gelatinous protection has developed or when this
    gelatinous matrix is removed.

         In a flow-through study, Hatakeyama (1987) exposed the chironomid
     Polypedilum nubifer, from the egg stage, to cadmium chloride. There
    was no effect on total number of adults, emergence success, sex ratio,
    total number of egg clusters, oviposition success or hatchability at
    10 µg cadmium/litre. There was a significant decrease in the total
    number of adults and emergence success at 20 µg/litre or more and in
    the total number of egg clusters at 40 µg/litre or more. At 80
    µg/litre survival and reproduction were very significantly depressed.
    In a separate experiment midges were fed cadmium-contaminated food
    (dried yeast) at concentrations of 22, 220, and 1800 mg cadmium/kg.
    Emergence success was decreased at 220 and 1800 mg/kg but no other
    effects were observed.

    6.2.4  Physiological and biochemical effects

         Berglind (1986) investigated the effect of cadmium alone and in
    combination with other metals on the delta-aminolevulinic acid
    dehydratase (ALAD) activity of  Daphnia magna. ALAD activity was
    enhanced by cadmium alone (at 2 µg/litre but not at 0.2 µg/litre) but
    this enhancement was abolished in the presence of zinc at 200
    µg/litre.

         Vernberg et al. (1977) investigated sub-lethal concentrations of
    cadmium and their effects on the adult shrimp  Palaemonetes pugio
    under static and flow-through conditions. Adult shrimps were exposed
    to cadmium at 50 µg/litre. This shrimp is highly tolerant to cadmium
    and after exposure to 23 mg/litre the mortality rate was only 10%. The
    authors found increased uptake of cadmium into the body of the shrimps
    with decreasing salinity. Similarly, at higher salinity levels,
    toxicity was lower. In shrimps kept at the lowest salinity level (5%),
    where cadmium body burden reached 40 mg/kg, there was inhibition of
    moulting. At more moderate cadmium body burdens of 23 mg/kg and 10
    mg/kg, observed at salinities of 10% and 20%, respectively, moulting
    was stimulated by the presence of cadmium. An investigation of the
    effects of cadmium on respiratory rate was inconclusive because of
    considerable variation. The authors considered that the flow-through
    system more nearly approximated field conditions than the static
    system. The relationship between salinity and cadmium uptake was
    eliminated in a static system at 15 °C, but was quite clearly present
    when the system was flow-through. After an extensive study on the
    effects of cadmium on three species of shrimps,  Penaeus duorarum,
     Palaemonetes pugio, and  Palaemonetes vulgaris, Nimmo et al. (1977)
    reported sublethal histological effects and blackening and damage to
    gill filaments. Placing shrimps with blackened gills in cadmium-free
    water resulted in the sloughing-off of blackened portions of the
    branchia and the shrimps appeared normal within 14 days. The effect on
    the gills occurred with exposure to cadmium concentrations approaching
    the LC50 which, with an exposure duration of 96 h, was 0.76 mg/litre
    for  Palaemonetes vulgaris and 3.5 mg/litre for  Penaeus duorarum.

    Thurberg et al. (1973) exposed two species of crabs ( arcinus maenus
    and  Cancer irroratus) to various concentrations of cadmium chloride
    for 48 h and at five different salinities. At the end of each exposure
    period, tests of blood serum osmolarity and gill tissue oxygen
    consumption were performed. Cadmium increased the osmolarity of
     Carcinus serum above its normal hyperosmotic state and reduced
    oxygen consumption by the gill tissue of both species. Effects on
    oxygen consumption were dose related over a range of cadmium
    concentrations from 0 to 4 mg/litre.

         Cadmium has been shown to cause an increase in oxygen consumption
    rates in the mud snail  Nassarius obsoletus at concentrations of
    between 0.5 and 4.0 mg/litre over a 72-h exposure period (MacInnes &
    Thurberg, 1973). A similar increase in oxygen consumption rate was
    observed in the marine snail  Murex trunculus during chronic exposure
    to 0.05 mg cadmium/litre (Dalla Via et al., 1989) and in crabs
    ( Callinectes similis) exposed to cadmium concentrations of between
    2.48 and 10.05 mg/litre for up to 96 h (Ramirez et al., 1989).

    6.2.5  Behavioural effects

         Olla et al. (1988) monitored the burrowing behaviour of three
    polychaete species,  Nereis virens,  Glycera dibranchiata, and
     Nephtys caeca during a 28-day exposure to a sediment concentration
    of 40 mg cadmium/kg. Most comparisons of burrowing times and rates
    between exposed and unexposed worms were not statistically
    significant. Four out of 15 comparisons gave significant results but
    these were randomly spread amongst species and exposure periods. The
    authors concluded that these results would probably have little
    ecological significance. The feeding behaviour of  G. dibranchiata
    was also monitored but no significant effect of the cadmium treatment
    was found.

    6.2.6  Interactions with other chemicals

         Sunda et al. (1978) carried out experiments in diluted sea water
    with various concentrations of the chelating agent nitrilotriacetic
    acid (NTA) to determine the relationship between the chemical
    speciation of cadmium and the toxicity of the metal to the grass
    shrimp  Palaemonetes pugio. After 4 days of exposure to a given
    concentration of cadmium chloride, shrimp mortality decreased with
    increasing salinity and increasing concentration of the chelating
    agent. The protective effect of high salinity or NTA was attributable
    to complexation of cadmium; mortality was related to the measured free
    cadmium ion concentration, which was determined by measuring total
    concentration of cadmium and deducting the calculated level of
    complexation by either the chloride ion or NTA. The mortality at a
    free cadmium ion concentration of approximately 4 x 10-7 mol/litre
    was 50%. In a study of the combined effects of zinc and cadmium on the
    shrimp  Callianassa australiensis by Negilski et al. (1981), there
    was interaction between the two metals; in combination they gave
    greater mortality than would be expected if there were no interaction.
    The authors demonstrated that each metal increased the accumulation of
    the other.

    6.2.7  Tolerance

         Khan et al. (1988) exposed two different populations of grass
    shrimp  Palaemonetes pugio to cadmium under static conditions and
    calculated 96-h LC50 values of 3.28 mg/litre for shrimps from an
    industrialized area and 1.83 mg/litre for those from a non-
    industrialized area. Pre-exposure of shrimps to 0.05 mg cadmium per
    litre caused an increase in the LC50 values to 6.81 and 3.89
    mg/litre for the two respective populations.

         Moraitou-Apostalopoulou et al. (1982) collected the shrimp
     Palaemon elegans from two different areas with different natural
    concentrations of cadmium and investigated the sublethal effects of
    the metal. They found that cadmium decreased respiration rates in the
    shrimp at sublethal concentrations. Shrimps sampled from an area with
    a natural cadmium concentration of 0.6 µg/litre were more tolerant to
    the metal than were those from an area with 0.1 µg/litre. There was
    also a difference in the acute toxicity of cadmium to the two
    populations, indicating that tolerance had developed. In an earlier
    study (Moraitou-Apostolopoulou et al., 1979), similar development of
    tolerance was reported for a copepod  Acartia clausi.

         In a study of the toxicity of cadmium to the freshwater cyclopoid
    copepod  Tropocyclops prasinus mexicanus, Lalande & Pinel-Alloul
    (1986) sampled animals from three Quebec lakes, one polluted and two
    unpolluted with cadmium. The cultures from the two unpolluted lakes
    showed lower LC50 values in 48-h tests than the culture from the
    polluted lake. However, the polluted lake had a significantly higher
    hardness (120 mg calcium carbonate per litre) than the other two lakes
    (10 mg/litre).

    6.2.8  Model ecosystems

         Borgmann et al. (1989a) established a  Daphnia-phytoplankton
    model ecosystem and exposed it to cadmium sulfate at concentrations of
    1, 5 and 15 µg cadmium/litre. At 5 µg/litre the  Daphnia population
    collapsed after 9 weeks of treatment and chlorophyll levels increased.
    At 15 µg/litre the  Daphnia population collapsed after 5 weeks, but
    chlorophyll levels remained low. There appeared to be no effect on
    this model system at 1 µg/litre.

    6.3  Toxicity to Fish

         The toxicity of cadmium has been studied in a variety of fish
    species in both fresh and sea water at various temperatures and
    dissolved oxygen concentrations. Generally, increasing dissolved salt
    concentration decreases the toxicity, whereas increasing temperature
    increases it. An increase in the dissolved oxygen content of the water
    decreases the toxicity of cadmium to freshwater fish. Salmonids appear
    to be particularly susceptible to the metal. Sublethal effects have
    been reported, notably malformation of the spine.

    6.3.1  Acute and short-term toxicity

         The acute toxicity of cadmium to fish is summarized in Tables 11
    and 12. Pickering & Henderson (1966) calculated the LC50 values for
    five species of warm-water fish, some of which were tested in both
    soft and hard water. There was surprisingly little difference in
    fathead minnows ( Pimephales promelas) between the 24-h, 48-h, and
    96-h LC50 values, which in soft water, were 1.09, 1.09, and 1.05
    mg/litre, respectively. This species was very much more resistant to
    cadmium in hard water with 24-h, 48-h, and 96-h LC50 values of 78.1,
    72.6, and 72.6 mg/litre, respectively. The hardness for the two types
    of water was 20 and 360 mg CaCO3 per litre and the alkalinity 80 and
    300 mg/litre. The dissolved oxygen concentration was similar in the
    two types of water. However, the pH was 7.5 for soft water and 8.2 for
    hard water, this being an area of the pH range where speciation of
    cadmium undergoes major change. Bluegill sunfish, goldfish, and
    guppies showed a decrease in LC50 with increase in exposure duration
    from 24 to 96 h (Table 12), but these were tested only in soft water.
    The green sunfish  Lepomis cyanellus showed LC50 values in soft
    water of 7.84, 3.68, and 2.84 mg/litre with exposure durations of 24
    h, 48 h, and 96 h, respectively. This species was also tested in hard
    water, where, like the fathead minnow, it showed considerably less
    cadmium toxicity. The 24-h LC50 rose from 7.84 in soft water to 88.6
    mg/litre in hard water.

         Pickering & Gast (1972) determined a maximum acceptable toxicant
    concentration (MATC) for the fathead minnow  Pimephales promelas of
    between 37 and 57 µg cadmium/litre. The experimental concentration of
    57 µg/litre decreased survival of the developing embryos, this being
    the most sensitive life-stage, but at lower concentrations (between
    4.5 and 37 µg/litre) no adverse effect was found on survival, growth
    or reproduction. Carroll et al. (1979) investigated the protective
    effects of various constituents of hard water on the toxicity of
    cadmium to the brook trout ( Salvelinus fontinalis) and concluded
    that calcium, added as either the sulfate or carbonate, was the most
    significant source of protection. This protective effect was observed
    in the absence of significant cadmium precipitation. Magnesium,
    sulfate, and sodium ions and the carbonate system provided little or
    no protection. Calamari et al. (1980) found an influence of water
    hardness on the toxicity of cadmium to  Salmo gairdneri; 48-h LC50
    values increased from 91 µg/litre, with a hardness of 20 mg/litre in
    the test water, to 3700 µg/litre at a water hardness of 320 mg/litre.
    The 48-h LC50 of fish acclimatized to a hardness of 320 mg/litre and
    then tested at a hardness of 20 mg/litre was about 7 times higher than
    that of fish acclimatized and tested in the same soft water. There are
    two types of biological effects of hardness on the availability of
    cadmium to fish; one of them persists after acclimatization in hard
    water.

    
    Table 11.  Toxicity of cadmium to marine or estuarine fish
                                                                                                                                     
    Organism               Size/      Stat/  Temperature  Salinity  pH       Duration  LC50                  Reference
                           age        flow a   (°C)         (%)                (h)       (mg/litre) b
                                                                                                                                     
    Striped killifish      0.95 g     stat   20           20        8.0      24        125 n                 Eisler (1971)
      (Fundulus majalis)   0.95 g     stat   20           20        8.0      48        59 n                  Eisler (1971)
                           0.95 g     stat   20           20        8.0      96        21 n                  Eisler (1971)

    Mummichog              0.89 g     stat   20           20        8.0      24        > 100 n               Eisler (1971)
      (Fundulus            0.89 g     stat   20           20        8.0      48        > 100 n               Eisler (1971)
       heteroclitus)       0.89 g     stat   20           20        8.0      96        55 n                  Eisler (1971)
                           1.3 g      stat   20           20        7.8      24        220 n                 Eisler & Hennekey (1977)
                           1.3 g      stat   20           20        7.8      96        22 n                  Eisler & Hennekey (1977)
                           1.3 g      stat   20           20        7.8      168       22 n                  Eisler & Hennekey (1977)
                           1 day      stat   20           20                 48        16.2 (12.7-21.2) n    Middaugh & Dean (1977)
                           7 days     stat   20           20                 48        9 (6.4-12.5) n        Middaugh & Dean (1977)
                           14 days    stat   20           20                 48        32 (24.6-41.6) n      Middaugh & Dean (1977)
                           adult      stat   20           20                 48        60 (40-90) n          Middaugh & Dean (1977)
                           1 day      stat   20           30                 48        23 (19.2-27.6) n      Middaugh & Dean (1977)
                           7 days     stat   20           30                 48        12 (9.2-15.6) n       Middaugh & Dean (1977)
                           14 days    stat   20           30                 48        7.8 (5.6-10.3) n      Middaugh & Dean (1977)
                           adult      stat   20           30                 48        43 (33-56) n          Middaugh & Dean (1977)

    Sheepshead minnow      1.1 g      stat   20           20        8.0      24        100 n                 Eisler (1971)
      (Cyprinodon          1.1 g      stat   20           20        8.0      48        50 n                  Eisler (1971)
       variegatus)         1.1 g      stat   20           20        8.0      96        50 n                  Eisler (1971)

    Coho salmon            smolt      flow   11.2         28.3      7.9      96        1.5 (1.2-2.4) m       Dinnel et al. (1989)
      (Oncorhynchus
       kisutch)

    Yellow-eye mullet      1.49 g     flow   18.5         34.5      7.8      58        15.5 (12.2-19.8) m    Negilski (1976)
      (Aldrichetta         1.15 g     flow   18.6         34.8      7.8      120       14.3 (8.4-24.3) m     Negilski (1976)
       forsteri)

    Small-mouthed          1.36 g     flow   17.9         34.5      7.9      168       12.7 (8.3-19.4) m     Negilski (1976)
    hardyhead              1.12 g     flow   18.0         34.5      7.8      168       16.6 (13.3-20.7) m    Negilski (1976)
      (Atherinasoma microstoma)

    Table 11 (contd).
                                                                                                                                     
    Organism               Size/      Stat/  Temperature  Salinity  pH       Duration  LC50                  Reference
                           age        flow a   (°C)         (%)                (h)       (mg/litre) b
                                                                                                                                     
    Atlantic silverside    adult      stat   20           20                 48        13 (9-20) n           Middaugh & Dean (1977)
      (Menidia menidia)    adult      stat   20           30                 48        12 (8-16) n           Middaugh & Dean (1977)

    Tidewater silverside   larva      stat   26           22                 96        0.31 (0.25-0.38) n    Mayer (1987)
      (Menidia peninsulae)

    Shiner perch           adult      flow   13           30.1      7.8      96        11 (5-20) m           Dinnel et al. (1989)
      (Cymatogaster aggregata)
                                                                                                                                     

     a stat = static conditions (water unchanged for duration of test); flow = flow-through conditions (cadmium concentration
      in water continuously maintained)
     b organisms exposed to cadmium added as cadmium chloride; m = measured concentration; n = nominal concentration

    Table 12.  Toxicity of cadmium to freshwater fish
                                                                                                                                     

    Organism          Size/      Stat/  Temperature  Hardness d   pH       Duration   LC50e                Reference
                      age        flow a   (°C)         (mg/litre)          (h)        (mg/litre)
                                                                                                                                     
    Chinook salmon    juvenile   flow   11-13        20-22      7.0-7.3  96         0.001 (± 0.0007) f m Finlayson & Verrue (1982)
      (Onchorhynchus
       tshawytscha)

    Rainbow trout     juvenile   flow                           6.4-8.3  96         0.0066 g m           Hale (1977)
      (Salmo          5-15 g     stat   8.5-10.7     61-65      7.4      48         2.9 m                Pascoe et al. (1986)
       gairdneri)     5-15 g     stat   8.5-10.7     283-317    7.4      48         5.7 m                Pascoe et al. (1986)
                      5-15 g     stat   8.5-10.7     61-65      7.4      96         1.3 m                Pascoe et al. (1986)
                      5-15 g     stat   8.5-10.7     61-65      7.4      96         2.6 m                Pascoe et al. (1986)

    Fathead minnow    adult      stat   25           20         7.5      24         1.09 (0.79-2.91) n   Pickering & Henderson (1966)
      (Pimephales     adult      stat   25           360        8.2      24         78.1 (57.2-117) n    Pickering & Henderson (1966)
       promelas)      adult      stat   25           20         7.5      48         1.09 (0.79-2.91) n   Pickering & Henderson (1966)
                      adult      stat   25           360        8.2      48         72.6 (52.7-105) n    Pickering & Henderson (1966)
                      adult      stat   25           20         7.5      96         1.05 (0.7-4.43) n    Pickering & Henderson (1966)
                      adult      stat   25           360        8.2      96         72.6 (52.7-105) n    Pickering & Henderson (1966)
                      adult      stat   18-22        190-210    7.7      48         0.1 (0.07-0.17) n    Hall et al. (1986)
                      adult      stat   18-22        190-210    7.7      96         0.09 (0.07-0.14) n   Hall et al. (1986)

    Bluegill sunfish  adult      stat   25           20         7.5      24         4.56 (3.64-6.08) n   Pickering & Henderson (1966)
      (Lepomis        adult      stat   25           20         7.5      48         2.76 (2.02-3.46) n   Pickering & Henderson (1966)
       macrochirus)   adult      stat   25           20         7.5      96         1.94 (1.33-2.35) n   Pickering & Henderson (1966)

    Goldfish          adult      stat   25           20         7.5      24         3.46 (2.85-4.82) n   Pickering & Henderson (1966)
      (Carassius      adult      stat   25           20         7.5      48         2.62 (2.04-3.68) n   Pickering & Henderson (1966)
       auratus)       adult      stat   25           20         7.5      96         2.34 (1.81-3.16) n   Pickering & Henderson (1966)

    Table 12 (contd).
                                                                                                                                     

    Organism          Size/      Stat/  Temperature  Hardness d   pH       Duration   LC50e                Reference
                      age        flow a   (°C)         (mg/litre)          (h)        (mg/litre)
                                                                                                                                     
    Guppy             adult      stat    25           20         7.5      24         3.37 (2.73-4.81) n   Pickering & Henderson (1966)
      (Poecilia       adult      stat    25           20         7.5      48         2.31 (1.78-3.11) n   Pickering & Henderson (1966)
       reticulata)    adult      stat    25           20         7.5      96         1.27 (0.97-1.71) n   Pickering & Henderson (1966)
                      3-4 weeks  flow c  23-25        1 mM                24         10.4 m               Canton & Slooff (1982)
                      3-4 weeks  flow c  23-25        1 mM                48         5.7 m                Canton & Slooff (1982)
                      3-4 weeks  flow c  23-25        1 mM                72         4.3 m                Canton & Slooff (1982)
                      3-4 weeks  flow c  23-25        1 mM                96         3.8 m                Canton & Slooff (1982)
                      3-4 weeks  flow c  23-25        2 mM                24         33 m                 Canton & Slooff (1982)
                      3-4 weeks  flow c  23-25        2 mM                48         20.5 m               Canton & Slooff (1982)
                      3-4 weeks  flow c  23-25        2 mM                72         14.4 m               Canton & Slooff (1982)
                      3-4 weeks  flow c  23-25        2 mM                96         11.1 m               Canton & Slooff (1982)

    Green sunfish     adult      stat    25           20         7.5      24         7.84 (6.13-14.2) n   Pickering & Henderson (1966)
      (Lepomis        adult      stat    25           360        8.2      24         88.6 (74-106) n      Pickering & Henderson (1966)
       cyanellus)     adult      stat    25           20         7.5      48         3.68 (2.89-4.69) n   Pickering & Henderson (1966)
                      adult      stat    25           360        8.2      48         71.3 (56.3-92.2) n   Pickering & Henderson (1966)
                      adult      stat    25           20         7.5      96         2.84 (2.1-3.56) n    Pickering & Henderson (1966)
                      adult      stat    25           360        8.2      96         66 (51.7-84.4) n     Pickering & Henderson (1966)

    Golden shiner                flow                 72.2       7.5      96         2.8 (1.9-4.3) m      Hartwell et al. (1989)
      (Notemigonus
       crysoleucas)

       Puntius        2.4 g      stat b   23-27        60-70      7.5      24         59.99 (58.5-61.5) n  Shivaraj & Patil (1988)
       arulius        2.4 g      stat b   23-27        60-70      7.5      48         45.7 (43.9-47.5) n   Shivaraj & Patil (1988)
                      2.4 g      stat b   23-27        60-70      7.5      72         41.7 (39.7-43.8) n   Shivaraj & Patil (1988)
                      2.4 g      stat b   23-27        60-70      7.5      96         39 (36.5-41.7) n     Shivaraj & Patil (1988)

    Table 12 (contd).
                                                                                                                                     

    Organism          Size/      Stat/  Temperature  Hardness d   pH       Duration   LC50e                Reference
                      age        flow a   (°C)         (mg/litre)          (h)        (mg/litre)
                                                                                                                                     
    Killifish         4-5 weeks  stat b   23-25        1 mM                48         > 2.8 m              Canton & Slooff (1982)
      (Oryzias        4-5 weeks  stat b   23-25        1 mM                72         0.35 m               Canton & Slooff (1982)
       latipes)       4-5 weeks  stat b   23-25        1 mM                96         0.35 m               Canton & Slooff (1982)
                      4-5 weeks  stat b   23-25        2 mM                24         > 2.6 m              Canton & Slooff (1982)
                      4-5 weeks  stat b   23-25        2 mM                48         1.8 m                Canton & Slooff (1982)
                      4-5 weeks  stat b   23-25        2 mM                72         0.17 m               Canton & Slooff (1982)
                      4-5 weeks  stat b   23-25        2 mM                96         0.13 m               Canton & Slooff (1982)

    Zebra fish        6 months   flow     19-21        1.7 mM              24         7 m                  Canton & Slooff (1982)
      (Brachydanio    6 months   flow     19-21        1.7 mM              48         4.2 m                Canton & Slooff (1982)
       rerio)
                                                                                                                                     

     a stat = static conditions (water unchanged for duration of test unless stated otherwise); flow = flow-through conditions
      (cadmium concentration in water continuously maintained unless stated otherwise)
     b static conditions but water renewed every 24 h
     c intermittent flow-through conditions
     d Hardness was expressed as mg CaCO3/litre unless stated otherwise
     e fish were exposed to cadmium added as the chloride unless stated otherwise; m = measured concentration; n = nominal concentration
     f cadmium was added as the sulfate
     g cadmium was added as the nitrate

    
         In a large scale study of the toxicity of cadmium to the
    mummichog  Fundulus heteroclitus, Voyer (1975) examined effects of
    salinity, pre-exposure to high salinity and different concentrations
    of dissolved oxygen on the tolerance of fish to cadmium over 96 h. He
    found no significant influence of dissolved oxygen levels between 4.0
    mg/litre and saturation regardless of salinity during acclimatization
    or during the test. By contrast, Voyer et al. (1975) showed a distinct
    effect of dissolved oxygen concentration on toxicity of cadmium to the
    same species of fish in fresh water. Median tolerance concentrations
    at 96 h ranged upwards from 1.3 to 3.0 mg cadmium/litre with 2.3 and
    8.5 mg/litre of dissolved oxygen, respectively. They demonstrated
    statistically an independent effect of dissolved oxygen and time
    against cadmium toxicity. It should be noted that cadmium is 10 times
    more toxic to this species in fresh water than in sea water.

         Toxicity of cadmium to both marine (Eisler, 1971) and freshwater
    (Roch & Maly, 1979) fish has been shown to be greater at higher
    temperatures.

         Canton & Slooff (1982) exposed several fish species to cadmium in
    short-term toxicity tests. At a water hardness of 1.7 mmol/litre they
    found the no-observed-adverse-effect level (NOAEL) for mortality in
    the zebra fish ( Brachydanio rerio) to be 2 mg/litre over a 48-h
    exposure period. For the killifish ( Oryzias latipes), the 96-h NOAEL
    was 0.06 mg/litre for mortality and 0.03 mg/litre for mortality  and
    abnormal behaviour at a water hardness of 2 mmol/litre. The
    corresponding values at a water hardness of 1 mmol/litre were 0.055
    and 0.006 mg/litre. For the guppy ( Poecilia reticulata), the 96-h
    NOAEL for mortality and abnormal behaviour was 5.2 mg/litre at a water
    hardness of 2 mmol/litre and 0.6 mg/litre at 1 mmol/litre. The authors
    calculated a 24-h NOAEL for the rainbow trout ( Salmo gairdneri) of
    0.01 mg/litre for inhibition of opercular movements.

         Abel & Papoutsoglou (1986) studied the toxicity of cadmium to
     Cyprinus carpio and  Tilapia aurea and reviewed data on other
    species of freshwater fish. The found for all species examined that
    the median survival time changed little over a wide range of cadmium
    concentrations and that a toxic threshold was clear in most studies.
    For  Tilapia this threshold lay between 0.1 and 0.5 mg cadmium/litre;
    negligible mortality was recorded in fish exposed to 0.1 mg/litre for
    3 months.

    6.3.2  Reproductive effects and effects on early life-stages

         Meteyer et al. (1988) exposed sheepshead minnow ( Cyprinodon
     variegatus) eggs to cadmium concentrations of between 0.39 and 1020
    µg/litre from approximately 4 h after fertilization. Hatching was
    delayed by up to 3 days at the highest cadmium concentration. All
    treated larvae were shorter than controls, but there was no
    dose-related effect of cadmium on growth.

         Middaugh & Dean (1977) examined the toxicity of cadmium to
    various life-stages of the mummichog  Fundulus heteroclitus. In 48-h
    tests, eggs were highly resistant to cadmium. The greatest effect (54%
    non-emergence) occurred at a cadmium concentration of 32 mg/litre; the
    control non-emergence was 17%. Newly-emerged larvae were less
    sensitive to cadmium than were 7-day-old larvae. There was an effect
    of salinity on the sensitivity of 14-day-old larvae to the metal
    (Table 11). Adults were less sensitive to cadmium than were larvae.
    Similar results were obtained with the Atlantic silverside ( Menidia
     menidia), larvae being the most sensitive life-stage. Weis & Weis
    (1977) found no effect of cadmium, at concentrations up to 10
    mg/litre, on embryos of  Fundulus heteroclitus. Rombough & Garside
    (1982) found the most sensitive indicator of cadmium toxicity to early
    life-stages of the Atlantic salmon ( Salmo salar) to be inhibition of
    growth of alevins, where significant reductions occurred with cadmium
    concentrations of 0.47 µg/litre. The LC50 for the interval between
    fertilization and viable hatch lay between 300 and 800 µg per litre.
    Newly hatched alevins showed a 24-h LC50 of between 1.5 and 2.4
    mg/litre. Sensitivity increased sharply in late alevins and
    significant mortality was recorded at a concentration of 8.2 µg/litre.

         Eaton et al. (1978) exposed embryos and larvae of seven
    freshwater fish species to nominal cadmium concentrations of 0, 0.4,
    1.2, 3.7, 11.6, 33.3, and 100 mg/litre for periods ranging from 3 to
    126 days. Actual concentrations were monitored and used in the
    assessment of the results. Results were expressed in terms of
    "standing crop", which the authors estimated as the product of the
    proportion of fish surviving and their total biomass. The lowest
    concentration of cadmium at which the standing crop was significantly
    different from controls was approximately 12 µg/litre for the white
    sucker, northern pike, smallmouth bass, west coast coho salmon, lake
    trout, and brown trout exposed as embryos or larvae for up to 64 days.
    The value was lower for brook trout (0.48 µg per litre) after exposure
    of larvae/juveniles for 65 days and for Lake Superior coho salmon (3.4
    µg/litre) after exposure of larvae/juveniles for 27 days. The highest
    cadmium concentration at which standing crop was not significantly
    different from controls varied for the seven species between 1.1 and
    4.2 µg/litre.

         Woodall et al. (1988) exposed rainbow trout ( Salmo gairdneri)
    fry to cadmium concentrations of 0, 0.1, 1.0 or 5.0 mg/litre for up to
    90 h. In preliminary experiments, they calculated that the 90-h LC50
    lay between 0.1 and 1.0 mg/litre. Pre-treatment of trout fry with
    cadmium initially had little effect (up to 30 h). However, with
    exposure periods of between 45 and 90 h, some protection was induced
    by pre-treatment. Benoit et al. (1976) exposed three generations of
    brook trout ( Salvelinus fontinalis) to concentrations of total
    cadmium varying between 0.06 and 6.4 µg/litre. Significant numbers of
    first and second generation adult males died during spawning when
    exposed to 3.4 µg/litre. This concentration also significantly
    retarded the growth of juvenile second and third generation offspring,
    but at a concentration of 1.7 µg/litre these effects were not seen.

         In a study by Borgmann & Ralph (1986), white sucker larvae
     Catostomus commersoni and young common shiners  Notropis cornutus
    were exposed to cadmium chloride at concentrations ranging from 6.24
    to 200 µg cadmium/litre. The relative growth rate of fish was
    significantly reduced at concentrations of 36 µg/litre or more in the
    case of suckers and 63 µg/litre or more in the case of shiners.
    Cadmium had no effect on the relative feeding rates.

         Hatakeyama & Yasuno (1987) studied the chronic effects of cadmium
    on the reproduction of the guppy  Poecilia reticulata. The fish were
    exposed to cadmium via cadmium-accumulated midge larvae used as their
    food source. The cumulative numbers of fry produced by guppies fed
    midge larvae containing 500, 800 or 1300 mg cadmium/kg for 6 months
    decreased to 79%, 65%, and 55% of the controls, respectively. At the
    highest dose, the mortality of females was significantly elevated at
    6 months, but no such effect was observed with the males.

         Michibata (1981) reported a protective effect of water hard-ness
    against the effects of cadmium on the eggs of  Oryzias latipes.

    6.3.3  Metabolic, biochemical and physiological effects

         Protective metal-binding proteins (metallothioneins) are induced
    by cadmium in fish (chapter 4).

         A manifest symptom of cadmium toxicity in freshwater fish is
    ionic imbalance with reduced plasma Ca2+, Na+, and CL-. The
    probable explanation is that cadmium is a potent inhibitor of
    ion-transporting enzymes. Verbost et al. (1988) showed that cadmium
    inhibited Ca-ATPase in the cell membranes of fish gut. It probably
    does the same in the gills because cadmium exposure has been shown to
    inhibit calcium uptake in the gills of adults (Verbost et al., 1987;
    Reid & McDonald, 1988) as well as in larvae (Wright et al., 1985).
    Similarly, cadmium has been shown to inhibit Na/K-ATPase in fish gills
    (Watson & Benson 1987), which, taken with the fact that cadmium
    probably also affects the production of ATP in the gills (Dickson et
    al., 1982), could explain the reduction of plasma Na+. Huiguang Fu
    (1989) studied the role of the hormones prolactin and cortisol in
    correcting cadmium-induced impairment of the calcium balance in
    tilapia ( Oreochromis mossambicus). Fish were able to recover from
    initial hypocalcaemia during a 35-day exposure to a concentration of
    10 µg cadmium/litre. This recovery involves prolactin-induced
    stimulation of active Ca2+ uptake and reduction of passive Ca2+
    efflux, together with cortisol-induced changes in chloride cells and
    stimulation of metallothionein synthesis in the liver, kidney, and
    gills. The author stated that the capacity to survive prolonged
    exposure to 10 µg cadmium/litre through physiological adaptation does
    not indicate that this cadmium concentration is acceptable to tilapia.
    Adaptation may be achieved at the expense of other essential processes
    like growth and reproduction.

         Arillo et al. (1984) investigated the effect of cadmium at levels
    of 1-10 µg/litre (concentrations above the water quality criteria
    value of 0.75 µg/litre proposed for salmonids by EIFAC/FAO) on a wide
    variety of biochemical parameters in the rainbow trout  (Salmo
     gairdneri). The exposure period was 4 months. Only at the highest
    test concentration of 10 µg/litre were there any effects on the fish,
    and then only on liver aminolevulinic acid dehydratase activity. The
    authors concluded that the water quality criterion was realistic.

         Dawson et al. (1977) exposed juvenile striped bass ( Morone
     saxatilis) to cadmium chloride concentrations of 0.5, 2.5 or 5
    µg/litre for 30 to 90 days, and the fish were then allowed to recover
    for 30 days in clean, running sea water. There was an inhibition of
    gill tissue respiration at 30 and 90 days, which recovered during the
    30-day period with clean water. The activities of the various enzymes
    measured were not affected. MacInnes et al. (1977) reported reduced
    gill tissue oxygen consumption in cunner ( Tautogolabrus adspersus)
    exposed to cadmium (0.05 or 0.1 mg/litre) for 30 or 60 days. They also
    reported a reduced activity of aspartate aminotransferase and an
    increased activity of glucose-6-phosphate dehydrogenase in the liver
    of the fish after 30 days of exposure to cadmium. Gill & Pant (1983)
    measured levels of various blood and tissue constituents after acute
    (24 h) or chronic (90 day) exposure to cadmium. Acute exposure to
    12.65 mg/litre led to significant hyperglycaemia and an increase in
    liver, kidney, and ovarian cholesterol levels. Chronic exposure to
    0.63 or 0.84 mg/litre, by contrast, led to an enduring hypoglycaemia
    and diminished levels of cholesterol in tissues. Both acute and
    chronic exposure to cadmium caused marked hypocholesterolaemia,
    glycogenolysis in the liver and brain and a rise in myocardial
    glycogen. Testis cholesterol was depleted after 60 days in both acute
    and chronic exposures.

         Sastry & Subhadra (1983) exposed the catfish  Heteropneustes
     fossilis to cadmium in the water at the sublethal concentration of
    2.3 µmol/litre for 15 or 30 days. The cadmium caused reduced
    absorption of glucose and fructose from the gut, this effect being
    more pronounced after 30 days of exposure than after 15 days. Filling
    intestinal sacs,  in vivo, with cadmium solutions (1 µmol per litre)
    reduced absorption of the sugars significantly over 1 h.

         Merlini (1978) pre-treated immature sunfish ( Lepomis gibbosus)
    with cadmium (0.004 mg/litre) and then fed treated and control fish
    with a single ration containing 58Co-labelled vitamin B12. The
    fish were subsequently fed non-radioactive food for 31 days before
    sacrifice. The author reported that cadmium-treated fish stored
    significantly less vitamin B12 in the liver than did controls.

         Carrier & Beitinger (1988a) studied the effect of cadmium on the
    critical thermal maximum (the temperature at which loss of equilibrium
    is coupled with loss of righting response) in the red shiner
    ( Notropis lutrensis) and fathead minnow ( Pimephales promelas). The
    red shiner was exposed to sublethal cadmium concentrations of 4.88,

    5.07, and 5.46 mg/litre and the fathead minnow to 0.09, 0.48, and 1.26
    mg/litre. Critical thermal maxima were significantly reduced for both
    species over a 10-day exposure period. The effect was found to be dose
    and time dependant. In the green sunfish ( Lepomis cyanellus) there
    was no effect of cadmium concentrations of 2.76, 4.22 or 5.17 mg/litre
    on the critical thermal maximum (Carrier & Beitinger, 1988b).

    6.3.4  Structural effects and malformations

         When Bengtsson et al. (1975) exposed 180 minnows ( Phoxinus
     phoxinus) to various concentrations of cadmium ranging from 7.5
    µg/litre to 4.8 mg/litre for 70 days, 31 of the 101 fish that survived
    developed lesions in the spinal column. Fractured vertebrae occurred
    in the caudal end of the abdominal section of the spine or in the
    caudal section; 64% of all fractures occurred in the first 7 caudal
    vertebrae and 21% occurred in abdominal vertebrae numbers 8 to 14.
    Hiraoka & Okuda (1984) cultured medaka ( Oryzias latipes) eggs in a
    cadmium solution of 0.01 mg/litre for 1 week and then investigated
    abnormalities in the vertebrae of the hatched fry, which were reared
    in clean water. There was no damage to the centra of the vertebrae in
    newly hatched fry. However, centrum-damaged fish were found in the
    first week and the numbers increased rapidly up to the 4th week after
    hatch. The cumulative frequency of vertebral-damaged fish was 13% and
    14% in the 5th and 6th weeks, respectively, and seemed to remain
    constant after this. Muramoto (1981b) reported that fish showing
    malformations of the spine after cadmium treatment had significantly
    less calcium in the vertebral column than did control fish.

         Voyer et al. (1975) found no short-term histopathological effects
    of cadmium, but long-term exposure to 28 mg/litre caused necrosis and
    sloughing of the mucosa of gills. Tissue damage was also evident in
    the nasal passages and buccal cavity. This histopathological effect
    was seen between exposure times of 512 and 612 h, but not before.

    6.3.5  Behavioural effects

         Hartwell et al. (1989) studied the avoidance response of the
    golden shiner ( Notemigonus crysoleucas) to cadmium concentrations of
    up to 68 µg/litre, but found no significant avoidance.

         Sullivan et al. (1978b) subjected fathead minnows ( Pimephales
     promelas) to acute (24 h) or subacute (21 days) exposure at
    sublethal cadmium concentrations and then placed them in experimental
    chambers with largemouth bass ( Micropterus salmoides), a fish which
    preys upon them. The minnows displayed altered behaviour patterns,
    including abnormal schooling behaviour, and were more vulnerable to
    predation than controls. The lowest acute cadmium exposure level that
    increased vulnerability was 0.375 mg/litre and the lowest subacute
    level 0.025 mg/litre. The authors pointed out that the subacute value
    of 0.025 mg/litre was well below reported no-effect levels of cadmium
    for fathead minnows established with respect to survival and
    reproductive effects. The avoidance threshold for cadmium in water by

    the rainbow trout ( Salmo gairdneri) is 50 µg/litre (Black & Birge,
    1980), which is 50 times higher than the 96-h LC50 value reported
    for this species.

    6.3.6  Interactions with other chemicals

         Muramoto (1981a) showed that the chelating agents EDTA and DPTA
    afforded some protection against the effects of cadmium on carp
    ( Cyprinus carpio) exposed to 0.05 or 0.1 mg cadmium/litre for 3
    months. There were effects on the vertebrae of exposed fish.

         Chelating agents that form hydrophobic complexes with heavy
    metals increase the bioavailability of the metal to aquatic organisms.
    Examples of these are xanthates and dithiocarbamates. Xanthates are
    used in the mining industry in the flotation process to refine metal
    from sulfide ores. As discussed in section 4.1, these compounds
    increase the uptake rate of cadmium through the gills in fish (Block
    & Part, 1986; Gottofrey et al., 1988; Block, 1991). Furthermore, they
    change the tissue distribution of the metal in such a way that more
    cadmium is found in lipid-rich tissues such as nervous tissue (brain)
    and adipose tissue than when fish are exposed to the metal alone.

         Finlayson & Verrue (1982) reported 96-h LC50 values for
    juvenile chinook salmon ( Onchorynchus tshawytscha) ranging from 0.6
    to 1.6 µg/litre. They found no synergistic or antagonistic toxic
    effects after combining cadmium and zinc in their test system. The
    results of tests were additive, the overall LC50 being a simple
    combination of individual metal effects at a zinc:cadmium ratio of
    1:0.008. Spehar et al. (1978b) exposed the flagfish  Jordanella
     floridae to cadmium and zinc, both individually and as a mixture, at
    concentrations ranging from 4.3 to 8.5 µg cadmium/litre and 73.4 to
    139 µg zinc/litre, through one complete life-cycle of the fish. There
    was no additive effect of cadmium and zinc at sublethal concentrations
    in mixed exposure. Effects on survival showed that the toxicity of
    cadmium and zinc mixtures was only slightly, if at all, greater than
    the toxicity of zinc alone. Anadu et al. (1989) reported that
    pre-exposure of rainbow trout ( Salmo gairdneri) to zinc (100
    µg/litre) for 17 days increased the subsequent 120-h LC50 for
    cadmium from 1.1 µg/litre to 4.1 µg/litre.

    6.4  Toxicity to Amphibia

         Francis et al. (1984) exposed eggs of the leopard frog ( Rana
     pipiens) to cadmium-enriched sediments during their development and
    for 4 days after the larvae had hatched. Measured concentrations of
    cadmium ranged from 1.04 to 1074 mg/kg in sediment and from 1.0 to
    76.5 mg/litre in water above the sediment. Cadmium concentrations in
    the tissues of the tadpoles at the end of the experiment ranged from
    0.08 to 12.55 mg/kg. There was no mortality as a result of cadmium
    exposure. The LC50 for this species has been reported to be 50
    µg/litre for water without sediment by Westerman (1977). Slooff &
    Baerselman (1980) determined 48-h LC50 values for the neotenous

    larval mexican axolotl ( Ambystoma mexicanum) and larval South
    African clawed toad ( Xenopus laevis) of 1.3 mg/litre and 32
    mg/litre, respectively, after exposure to cadmium nitrate. Canton &
    Slooff (1982) exposed  Xenopus laevis to cadmium, added as cadmium
    chloride, and obtained 24-h and 48-h LC50 values of 4 and 3.2
    mg/litre, respectively. A NOEL of 2.2 mg/litre was reported for both
    exposure periods. In a longer-term exposure (100 days), by the same
    authors, an LC50 value of 1500 µg/litre was found and the EC50
    value for inhibition of larval development was 650 µg/litre. For
    mortality and larval development, the NOELs were 30 and 9 µg/litre,
    respectively. De Zwart & Sloof (1987) determined a 48-h LC50 of 20.2
    mg/litre for tadpoles of the clawed toad. Khangarot & Ray (1987)
    established a 96-h LC50 value of 8.18 (6.96-9.53) mg/litre for the
    tadpoles of the toad  Bufo melanosticus. The test water was obtained
    from a well and had a hardness of 185 mg per litre, pH 7.4, and
    temperature of 31 °C. Solids were present at a level of 920 mg/litre.
    Muino et al. (1990) calculated the 48-h and 96-h LC50 for  Bufo
     arenarum tadpoles to be 2.52 and 2.08 mg cadmium/litre for the two
    exposure periods, respectively, under semi-static conditions. In tests
    to study the effect of a sublethal cadmium concentration (1.0 mg
    cadmium/litre) on the water balance of the animals, the authors found
    that all animals died within a few hours in ion-free media. Tadpoles
    exposed in ionic solutions showed mortality of less than 10%
    (equivalent to control groups).

         Woodall et al. (1988) exposed  Xenopus laevis tadpoles to
    cadmium concentrations of 0, 50, 80, and 100 mg cadmium/litre for up
    to 90 h. In preliminary experiments, they calculated the 90-h LC50
    to lie between 80 and 100 mg/litre. The authors found that
    pre-treatment of tadpoles with cadmium induced protection, which
    decreased with an increase in the subsequent exposure concentration.
    Cadmium pre-treatment induced maximum protection to cadmium at a
    concentration of 50 mg/litre at both 45 and 90 h.

         Perez-Coll et al. (1986) exposed developing  Bufo arenarum
    embryos to cadmium chloride concentrations of 6 x 10-7 to 1.5 x
    10-5 mol Cd2+/litre during gastrulation at 20 °C and 30 °C.
    Initial failures at gastrulation resulted mainly in axial
    incurvations, microcephaly, hydropsy, and abnormal tail development.
    At the higher temperature, high concentrations of cadmium caused a
    significant increase in early malformations and at low concentrations
    the high temperature prevented alterations.

    7.  TOXICITY TO TERRESTRIAL ORGANISMS

    Appraisal

          Both terrestrial plants and animals accumulate cadmium, but the
     rate of accumulation is much higher under experimental conditions,
     where cadmium is available in solution, than it is with plants grown
     in soil, when part of the cadmium is bound and less available.
     Cadmium has adverse effects on hydroponically grown plants at
     concentrations in the mg/litre range, whereas plants grown in soil
     only show reduced growth in contaminated soils with hundreds of mg
     cadmium/kg. Terrestrial invertebrates are relatively insensitive to
     cadmium-induced toxic effects, probably due to effective
     sequestration mechanisms in specific organs. When toxic effects do
     occur, they consist of reduced growth and reproduction.

    7.1  Toxicity to terrestrial plants

         Cadmium has been shown to have an adverse effect on plant growth
    and yield in laboratory experiments. However, plants grown in soil are
    generally insensitive to the effects of cadmium except at high doses.
    Effects are only seen when cadmium is given in nutrient solutions
    rather than in soil, where the cadmium is bound and is therefore less
    available to the plants. Cadmium is only available to plants in
    solution in soil. There is considerable evidence from field studies
    that plants are able to develop tolerance to various heavy metals in
    their growth medium. Research into cadmium tolerance has been more
    limited than for other metals, but there is some evidence of tolerance
    developing.

    7.1.1  Toxicity to plants grown hydroponically

         Mitchell & Fretz (1977) cultured seedlings of three species of
    tree, the white pine ( Pinus strobus), red maple ( Acer rubrum), and
    Norway spruce ( Picea abies), in sand. Plants were irrigated with a
    nutrient solution containing cadmium at concentrations of 0, 0.5, 1,
    2, 4, 8, and 16 µg/litre; white pine seedlings were also treated with
    32 and 64 µg/litre. Both roots and foliage were affected by the
    cadmium. In the red maple symptoms of cadmium toxicity began with
    interveinal chlorosis and stunting of leaves in most cases. As
    exposure increased cadmium caused wilting and then death. The first
    observed effect of the metal on the pine was inhibition of needle
    expansion and, in the case of the spruce, chlorotic tips to new
    growth. Tissue accumulation of cadmium correlated well with exposure.
    Red maple, white pine, and spruce exhibited foliage effects at leaf
    cadmium concentrations of 22.8, 61.3, and 7.5 mg/kg, respectively,
    corresponding to nutrient solutions of 8.0, 32.0, and 4.0 µg/litre.
    There was an increasing effect on root development with increasing
    exposure to cadmium. At the higher doses, there was severe reduction
    in the number of roots initiated and stunting of those that grew.
    Accumulation of cadmium was greater in roots than in leaves.

         Root et al. (1975) grew maize ( Zea mays) in hydroponic
    solutions containing cadmium chloride at concentrations ranging from
    1 to 40 mg/litre. Uptake of cadmium into the plants increased with
    time, and cadmium was present at higher concentrations in roots than
    in shoots. Leaf chlorophyll concentration and yield (as dry weight) of
    both roots and shoots decreased with increasing cadmium concentration.
    As the cadmium concentration in the leaves increased, the
    concentration of zinc decreased and the concentration of iron
    increased. This gave a linear correlation between cadmium in the leaf
    and iron/zinc ratio. Chlorosis resulting from cadmium in the leaves
    (seen at a cadmium concentration of 1 mg/litre nutrient solution)
    appeared comparable to iron-deficiency chlorosis. However, in this
    case, the chlorosis was not due to iron deficiency, as previously
    suggested by other workers, but was associated in some way with an
    increasing iron/zinc ratio.

         Harkov et al. (1979) found no effect on the yield of tomatoes
    grown in vermiculite and cultured with a nutrient solution containing
    cadmium at concentrations of 0.25 or 0.75 mg/litre. The plants were
    more susceptible to damage by ozone, under conditions where ozone
    damage would have been slight, after exposure to cadmium. Where ozone
    damage was heavy or when conditions were not conducive to ozone
    damage, there was no effect of cadmium. When Wong et al. (1988)
    exposed pea ( Pisum sativum) seeds to cadmium concentrations of 1, 5,
    10, and 20 mg/litre in culture solutions, germination was
    significantly reduced at 20 mg/litre and radicle elongation to 1 cm
    was significantly reduced at 5 mg/litre and to 2 cm at 1 mg/litre.
    Early development (shoot elongation, leaf development, root and shoot
    growth) was inhibited in a dose-dependant manner. Slight inhibition
    was observed at 1 mg/litre, increased inhibition at 5 mg/litre, and
    significant inhibition at 10 and 20 mg/litre.

    7.1.2  Toxicity to plants grown in soil

         Mitchell & Fretz (1977) showed that the effects on the growth of
    red maple, white pine and Norway spruce plants in soil, amended with
    cadmium, were similar but less severe, owing to reduced uptake of the
    metal, than in the case of the same plants grown hydroponically.
    Cadmium only affected current growth of the plants, except where it
    was present in excess. Mahler et al. (1978) treated eight soils, the
    pH values of which ranged from 4.8 to 7.8, with 1% (by weight) sewage
    sludge containing added cadmium sulfate, leading to cadmium
    concentrations in the soil ranging from 0.1 to 320 mg/kg. Two plants,
    lettuce ( Lactuca sativa variety longifolia) and Swiss chard ( Beta
     vulgaris variety cicla), were grown in the soils in pots. The EC50
    (yield) for lettuce was 214 and 139 mg/kg soil for acid and calcareous
    soils, respectively, whereas the values for chard were 175 and 250
    mg/kg for acid and calareous soils. The corresponding tissue
    concentrations of cadmium associated with these effects were 470 and
    160 mg/kg for lettuce and 714 and 203 mg/kg for chard. Thus, a
    markedly lower tissue concentration of cadmium produced 50% yield
    reduction on calcareous soils than on acid soils. Alloway et al.

    (1990) reported stunted growth and toxic signs on leaves of lettuce,
    cabbage, carrot, and radish plants, but only at the highest
    concentrations of cadmium tested (which resulted in a cadmium content
    of around 20 mg/kg in the upper parts of the plants).

    7.1.3  In vitro physiological studies

         Bazzaz et al. (1974) demonstrated an effect of cadmium on
    transpiration and photosynthesis in excised sunflower heads. The heads
    (15 cm diameter) were placed in flasks containing distilled water or
    cadmium salt solutions (2, 20, 100 or 200 mg/litre) and transpiration
    and photosynthesis were measured at daily intervals over 4 to 5 days.
    Cadmium reduced transpiration and photosynthesis at concentrations of
    100 or 200 mg/litre. Excised epidermal peels floating on solutions of
    cadmium salts showed a log-linear relationship between metal
    concentration and stomatal opening. The stomata opened less with
    increasing cadmium concentration; this accounted for the effect on
    transpiration and, hence, on photosynthesis.

    7.2  Toxicity to terrestrial invertebrates

         Haight et al. (1982) calculated 24-h, 48-h, and 72-h LC50
    values of 36, 15.1, and 5.85 mg cadmium/litre, respectively, for
    juvenile free-living nematodes ( Panagrellus silusiae) and 111, 26.3,
    and 13.2 mg/litre for adults. Williams & Dusenbery (1990) exposed the
    free-living nematode  Caenorhabditis elegans to cadmium and found
    values of 904, 22, and 1.5 mg/litre, respectively, for the same three
    exposure periods. They also calculated a 96-h LC50 of 0.06 mg/litre.

         Popham & Webster (1979) found that a 6-h exposure to 3.26 x
    10-7 moles of cadmium significantly decreased the fecundity of  C.
     elegans. A 3.5-day exposure to 10-8 moles caused the same effect.
    Nematodes exposed to 4 x 10-6 moles of cadmium never grew to the
    same length as controls and resembled worms from starved, overcrowded
    cultures. Van Kessel et al. (1989) exposed juvenile  C. elegans to
    various concentrations of cadmium chloride and found that growth and
    subsequent reproduction were significantly reduced at 1 µmol/litre. At
    levels of 160 and 320 µmol/litre the nematodes did not reach the adult
    stage and, therefore, did not reproduce.

         Doelman et al. (1984) exposed the soil nematodes  Mesorhabditus
     monhystera and  Aphelenchus avenae to cadmium via food for up to 22
    days and monitored the size of the population.  M. monhystera was
    exposed, via bacteria and fungi, to concentrations of 0.23, 4.4, and
    12.7 mg cadmium/kg, and a significant reduction in the size of the
    population was found at all doses.  A. avenae was exposed, via fungi
    alone, to concentrations of 1, 10, and 25 mg/kg. At 1 mg/kg there was
    no effect on the population size, whereas at 10 mg/kg, a reduction was
    observed until the final day. A concentration of 25 mg/kg
    significantly reduced the size of the population. The authors noted
    that exposure via fungi alone gave far more variable results.

         In studies by Van Straalen et al. (1989), the collembolan
     Orchesella cincta and the oribatid mite  Platynothrus peltifer were
    exposed to cadmium in the food. The 9-week LC50 values were 1.6 and
    7.27 µmol/g and the no-observed-effect levels (NOEL) were 0.042 and
    0.026 µmol/g for  O. cincta and  P. peltifer, respectively. The most
    sensitive parameters were female growth for  O. cincta and
    reproduction in  P. peltifer.

         Russell et al. (1981) fed subadult garden snails ( Helix aspersa)
    on diets containing six different levels of cadmium ranging from 10 to
    1000 mg/kg diet over a period of 30 days. There was little mortality
    (two animals out of 350 died, one at an exposure level of 50 mg/kg and
    the other at 1000 mg/kg) but food consumption declined with each
    increase in cadmium dose. Food consumption was strongly depressed at
    cadmium doses of 100 mg/kg or more. Relative weight loss was the most
    pronounced effect of cadmium treatment; this was dose related and
    directly attributable to reduced feeding rates. At doses of 25 mg/kg
    or more, shell growth and reproductive activity were depressed while
    the incidence of sealing response (the sealing of the operculum with
    a disc of mucus and a dormancy reaction) increased markedly. These
    three effects were all related to the dietary cadmium concentration.

    7.3  Toxicity to birds

    7.3.1  Acute and short-term toxicity

         The acute and short-term toxicity of cadmium salts to birds in
    laboratory studies is summarized in Table 13. Dosing for 5 days,
    followed by 3 days of clean diet, resulted in LC50 values generally
    in excess of 2000 mg/kg diet. Only the pheasant showed greater
    sensitivity to cadmium but, even in this species, the LC50 was close
    to 1000 mg/kg diet. All the birds used were between 10 and 14 days
    old.

        Table 13.  Toxicity of cadmium to birds a
                                                                                      
    Species                Age     Salt                LC50               Reference
                           (days)                      (mg/kg diet)
                                                                                      
    Japanese quail         14      cadmium chloride    2440 (1807-3294)   Hill &
       (Coturnix coturnix  14      cadmium succinate   2052 (1621-2598)   Camardese
       japonica)                                                          (1986)

    Pheasant               10      cadmium chloride    767 (651-898)      Hill et al.
      (Phasianus           14      cadmium succinate   1411 (1202-1657)   (1975)
       colchicus)

    Bobwhite quail         14      cadmium succinate   1728 (1381-2132)   Hill et al.
       (Colinus                                                           (1975)
       virginianus)

    Table 13 (contd).
                                                                                      
    Species                Age     Salt                LC50               Reference
                           (days)                      (mg/kg diet)
                                                                                      
    Mallard duck           10      cadmium chloride    > 5000             Hill et al.
       (Anas               10      cadmium succinate   > 5000             (1975)
       platyrhynchos)
                                                                                      

     a Birds were fed with a dosed diet for 5 days and then a "clean" diet for 3 days.

        In a study by Pritzl et al. (1974), 2-week-old leghorn chicken chicks
    were dosed with dietary cadmium chloride for 20 days. In the first
    experiment, chicks dosed with 700 mg cadmium/kg diet showed an
    increase in the weight of the gastrointestinal tract, kidney, and
    gizzard expressed as a ratio to the body weight. In a second
    experiment, chicks were fed diets containing 400, 600, 800 or 1000 mg
    cadmium/kg. Weight gain and food consumption were decreased, relative
    to controls, at all dose levels, and at levels higher than 400 mg/kg
    the birds lost weight. All the birds fed diets containing 800 or 1000
    mg/kg died within 20 days. The LC50 was calculated to be 565 mg/kg
    diet.

         When Cain et al. (1983) fed 1-day-old mallard ducklings ( Anas
     platyrhynchos) a diet containing cadmium chloride at concentrations
    of 5, 10 or 20 mg cadmium/kg for 12 weeks, significant effects were
    only noted at the highest dose. These included a significant reduction
    in packed cell volume and haemoglobin concentrations and a significant
    increase in serum glutamic-pyruvic transaminase. Mild to severe kidney
    lesions were evident in ducklings fed 20 mg/kg for 12 weeks. Body
    weight, liver weight, and femur weight-to-length ratio were unaffected
    by the cadmium treatment. No other haematological or histological
    effects were found.

    7.3.2  Reproductive effects

         Lofts & Murton (1967) injected 0.2 ml of a solution of cadmium
    chloride (0.04 mol/litre) intramuscularly into wood pigeons ( Columba
     palumbus). When the cadmium was given to birds with regressed
    testes, which were then stimulated into reproductive condition by long
    photoperiods (16 h of light per day), there was a reduction in the
    numbers of birds showing full testicular development in the treated
    group. Only one out of six birds given cadmium had developed
    spermatozoa in the testis by the end of the experiment. The remainder
    had not even produced spermatids; two birds had only spermatogonia in
    the seminiferous epithelium while the other three had secondary
    spermatocytes. Of the six control birds, four had spermatozoa, one had
    spermatids, and one primary spermatocytes. Injection of cadmium into
    birds late in the season had no effect on the autumnal regression of
    the testes. There was no sign of testicular necrosis in the treated

    birds. An intratesticular injection of cadmium caused local necrosis
    in the testis of feral pigeons. A dietary concentration of 200 mg
    cadmium/kg, in the form of cadmium chloride, reduced spermatogenesis
    in male mallards and egg production in females, but a lower dose of 20
    mg/kg produced no effects (White & Finley, 1978; White et al., 1978).

    7.3.3  Physiological effects

         Mayack et al. (1981) found that the survival and growth of the
    wood duck ( Aix sponsa) were unaffected by a cadmium chloride dietary
    level of 100 mg/kg, although some kidney damage was reported.

         Nicholson et al. (1983) compared the ultrastructure of the
    kidneys of sea-birds contaminated with cadmium in the wild, sea-birds
    from uncontaminated colonies, starlings dosed with cadmium in the
    laboratory, and control starlings. They found damage to kidney cells
    to be comparable between wild sea-birds and dosed starlings having
    kidney cadmium levels of 60-480 and 95-240 mg per kg, respectively.
    Damage was greatest in the proximal tubule of the kidney, and included
    cell necrosis, nuclear pyknosis, mitochondrial swelling, and some
    tubulorrhexis. The tubulorrhexis would be irreversible. There was some
    indication of regeneration, judging from the number of
    undifferentiated cells present in the tubule, in both dosed and
    naturally contaminated birds. Debris was found in the distal nephron
    lumen and there was some damage in the distal tubule and the renal
    corpuscles. Necrosis of kidney cells was very rare in control birds or
    uncontaminated sea-birds.

    7.3.4  Behavioural effects

         Heinz et al. (1983) assessed the avoidance response to a visual
    fright stimulus of ducklings fed a diet containing cadmium chloride at
    a concentration of 4 or 40 mg/kg. The parents of the ducklings had
    also been fed this cadmium-containing diet. Ducklings fed 4 mg/kg were
    hypersensitive to the fright stimulus, whereas those fed the higher
    dose reacted as did controls. The authors could offer no explanation
    of why the higher dose had no effect but pointed to similar results
    from other materials. They were of the opinion that hypersensitivity
    to behavioural signals could be as deleterious to the organism in the
    wild as a failure to respond.

    7.4  Toxicity to wild small mammals

         Shore et al. (1991) fed herbivorous bank voles ( Clethrionomys
     glareolus) and granivorous wood mice ( Apodemus sylvaticus) a
    pelleted diet contaminated with cadmium chloride and collected urine
    and faeces in metabolism cages. Bank voles fed diets containing 10.3
    mg/kg for 40 days and then 4.5 mg/kg for 35 days suffered significant
    net daily loss of calcium and sodium, and reduced net gain of
    potassium and magnesium compared to controls. Assimilation of the
    macroelements was not significantly altered in wood mice fed 10.3
    mg/kg for 75 days.

    8.  EFFECTS IN THE FIELD

    Appraisal

          Tolerance to cadmium has been demonstrated in soil fungi,
     plants, aquatic invertebrates, and fish from cadmium-contaminated
     sites. Some field evidence suggests that cadmium is responsible for
     reduced leaf litter degradation and a failure to recycle nutrients
     due to adverse effects on populations, particularly of
     microorganisms. However, no studies have identified cadmium as the
     sole cause of the effect, since it is always associated with other
     metals. Although soil invertebrates in contaminated sites accumulate
     cadmium and other metals, there is evidence that most populations are
     not affected. A field study has shown that fish from a
     cadmium-contaminated river have physiological abnormalities. Kidney
     damage has been found in pelagic sea-birds from areas away from
     industrial or other anthropogenic sources of cadmium, but there was
     no effect on survival or reproduction of populations. In industrially
     contaminated areas, kidney damage has been observed in several
     species of birds found to contain cadmium plus other metals.

    8.1  Tolerance

         Tolerance to cadmium has been demonstrated in soil fungi (section
    5.2), aquatic invertebrates (section 6.2.7), and plants collected from
    sites with high cadmium levels, such as those in the vicinity of
    metalliferous mines and smelters.

         Coughtrey & Martin (1977) experimentally demonstrated tolerance
    of the grass  Holcus lanatus to cadmium to be greater in plants
    collected from an area subject to high fall-out of cadmium than in
    plants collected from a control site. Growth of tolerant plants was
    reduced in uncontaminated culture solutions, relative to controls, but
    was similar to that of control plants in solutions where cadmium salts
    had been added at levels similar to the field exposure. Simon (1977)
    reported cadmium tolerance in the grasses  Festuca ovina and
     Agrostis tennuis. The tolerant grasses were collected from areas
    contaminated by mining and aerial fall-out of cadmium.

    8.2  Effects close to industrial sources and highways

         There have been several reports of effects of heavy metal
    deposition on the accumulation rate of leaf litter in deciduous
    woodlands. These effects are restricted to areas close to, or down
    wind from, smelter sites. The separation of the effects of cadmium
    from those of other heavy metals present in the litter is difficult.
    A study by Coughtrey et al. (1979) attempted to do this by detailed
    analysis of the litter itself and by the use of statistics to separate
    effects of different components of the pollution fall-out. Seven areas
    of woodland in the vicinity of, or up to 28 km away from, a
    lead-zinc-cadmium smelter in Avonmouth, United Kingdom, were studied.
    The leaf litter contained lead, zinc, copper, and cadmium (in that

    order of concentrations), and metal levels were high in samples taken
    from within 3 km of the smelter. Litter from a wood 6.8 km from the
    smelter had similar levels to control litter collected 30 km away, but
    the prevailing wind would not have carried much of the fall-out in the
    direction of this wood. For the four woods within 3 km of the smelter,
    cadmium levels ranged from 23 to 98 mg/kg litter (lead levels were
    between 721 and 2179 mg/kg, zinc levels between 764 and 2814 mg/kg,
    and copper levels between 47 and 135 mg/kg). The weight of litter
    accumulated per unit area was markedly greater in the contami-nated
    sites than in the uncontaminated ones; litter standing crop ranged
    from 7.91 to 13.16 kg/m2 in contaminated and from 0.913 to 3.104
    kg/m2 in uncontaminated sites. The litter accumulation correlated
    well with levels of all metals but not with the pH of the litter,
    which varied between 3.88 and 6.3 over the sites. Partial correlation
    analysis showed that cadmium and zinc interrelated; with both cadmium
    and zinc, partial correlation coefficients were highly significant
    when lead, copper or pH effects were accounted for. However,
    correlations were low for lead and copper when cadmium or zinc were
    accounted for. Of further interest was an analysis of cadmium and zinc
    in leaf litter from various sites. There was an increase in the
    smaller particle sizes in contaminated sites relative to
    uncontaminated ones. These smaller particles contained a
    disproportionate amount of the metals present, particularly in the
    case of cadmium. Litter standing crop and cadmium concentrations were
    highly correlated; the correlation between cadmium content and
    different particle sizes of litter was better for small particles
    sizes, and the slope of the regression line between cadmium
    concentration and litter weight decreased with increasing particle
    size. The authors argued that litter degradation was not affected at
    the early stages but only when breakdown had progressed to much
    smaller particle sizes. This perhaps supports the view that
    microorganisms are inhibited by metals to a greater extent than
    invertebrates, which would produce the initial reduction in size of
    litter fragments. Taking the figure of 900 g/m2 as the normal leaf
    litter level for woodland, the extra accumulation in contaminated
    woods represented 25 to 30 years of litter accumulation (the smelter
    in question had been operating for 48 years) and, possibly a large
    proportion of the total capital of nutrients normally recycled to the
    plants.

         Other authors have also reported accumulation of leaf litter in
    areas contaminated by metals (Tyler, 1972; Strojan, 1978), although
    they disagree about the probable cause. Strojan (1978) proposed that
    the effect relates to the absence of some groups of invertebrates,
    while Jordan & Lechavalier (1975) suggested that the effect is on
    microorganisms. There is no direct evidence that invertebrates in leaf
    litter are adversely affected by metals, although they do accumulate
    all the metals found in litter (Martin et al., 1976; Coughtrey &
    Martin, 1976). Both Tyler (1972) and Strojan (1978) argued that the
    productivity of woodland may be adversely affected by the failure to
    recycle nutrients in areas contaminated by heavy metals. Coughtrey et
    al. (1979) considered that the litter is an important sink for heavy

    metals, and that the result of litter organisms developing tolerance
    to the metals and, therefore, in the long-term increasing the rate of
    degradation is unpredictable since metals would be released at the
    same time as nutrients.

         In a study by van Straalen et al. (1987), the metal excretion
    efficiency of the collembolan  Orchesella cincta collected from
    various contaminated forest soils was monitored. The authors found
    that moderate to high soil cadmium contamination of industrial origin
    did not evoke increased cadmium excretion. In fact contamination
    initiated in this century from a zinc factory caused a significant
    decrease in excretion efficiency. Soils that had been contaminated
    with cadmium for many years (lead/zinc factory) or to an extreme
    degree (lead smelter) were inhabited by Collembola able to increase
    metal excretion.

         Muskett & Jones (1980) found levels of cadmium to be higher than
    normal within 10 m of a road with a heavy traffic, but no effect on
    the numbers of invertebrates caught or their species diversity was
    observed.

    8.3  Effects on fish

         Field studies in Sweden showed that perch ( Perca fluviatilis)
    from a cadmium-contaminated river (0.1 to 0.2 µg cadmium/litre) had
    physiological abnormalities similar to those shown in laboratory
    experiments (Sjobeck et al., 1984).

    8.4  Effects on sea-birds

         The reported effects on the kidney of sea-birds are not always a
    result of exposure to cadmium as an industrial pollutant, since the
    individuals most affected come from areas where there is no industrial
    effluent. This is often, therefore, a response to naturally occurring
    cadmium presumed to derive from the oceans. The birds appear to cope
    with this damage to the kidney and suffer no effects on survival or
    breeding success. No damage resulting from exposure to strictly
    anthropogenically derived cadmium appears to have been reported on the
    same scale as that from exposure to naturally occurring cadmium.
    Nicholson et al. (1983) compared the ultrastructure of the kidneys of
    sea-birds contaminated with cadmium in the wild, sea-birds from
    uncontaminated colonies, starlings dosed with cadmium in the
    laboratory, and control starlings. They found damage to kidney cells
    to be comparable between wild sea-birds and dosed starlings having
    kidney cadmium levels of 60-480 and 95-240 mg/kg, respectively (see
    section 7.3.3). Nicholson & Osborn (1983) reported kidney lesions
    (described in section 7.3.3) in several different species of sea-bird
    caught in contaminated areas, although other pollutant metals such as
    mercury were also present in the tissues.

    9.  EVALUATION

    9.1  General considerations

         In evaluating the environmental hazard of cadmium, it is
    necessary to extrapolate from laboratories studies to ecosystems. This
    must be done with extreme caution for a number of reasons.

    a)   The availability of cadmium to organisms in the environment is
         limited by its strong adsorption to environmental components such
         as soil, sediment, and organic matter. Organisms in contaminated
         areas accumulate high body burdens of cadmium.

    b)   Environmental variables such as temperature, pH, and the chemical
         composition of water or soil have been shown to affect both the
         uptake and the toxic impact of cadmium.

    c)   Available, rather than nominal or total, cadmium is the
         determinant in assessing uptake by, and effects on, organisms.

    d)   There are limited data from controlled experimental studies on
         the effects of mixtures of metals. Organisms in the environment
         are exposed to mixtures of pollutants. Acid deposition can
         release metals, including cadmium, into the environment.

    e)   Little experimental work has been carried out on species or
         communities that are either representative or key components of
         natural communities and ecosystems. Studies have not considered
         all of the interactions between populations and all of the
         environmental factors affecting these populations. As a result,
         the impact of cadmium on ecosystems may have been underestimated.

    f)   Results from laboratory studies based on very sensitive
         parameters may be indicative of physiological impacts on
         individuals rather than impacts on ecosystems.

    9.2  The aquatic environment

         Cadmium input to the aquatic environment is through dis-charge of
    industrial waste, surface run-off, and deposition. It is strongly
    adsorbed onto sediments and soils. The average cadmium content of sea
    water is about 0.1 µg/litre or less, while fresh waters contain <
    0.01 to 0.06 µg/litre in unpolluted areas. Cadmium levels of up to 5
    mg/kg and 0.03 to 1 mg/kg have been reported for freshwater sediments
    and marine sediments, respectively.

         The rate of uptake and the toxic impact of cadmium on aquatic
    organisms is greatly affected by physicochemical factors such as
    temperature, ionic concentration, and organic matter content.

         Cadmium is translocated by aquatic plants and concentrated in
    roots and leaves. It is also taken up and accumulated by various

    aquatic animals. The toxicity of cadmium to freshwater organisms
    varies considerably depending on the exposure duration, species, and
    life-stage. The early life-stages and the reproductive system are the
    most vulnerable. Cadmium is, by comparison, one of the most toxic
    heavy metals in the freshwater environment. Manifest responses of
    certain organisms to cadmium are observed at environmental
    concentrations lower than 1 µg/litre.

         Cadmium-induced kidney damage has been reported in sea-birds
    sampled from the field. However, this damage is present in both
    cadmium-polluted areas and areas remote from industrial contamination.
    The effect is probably, therefore, due to natural cadmium in certain
    species and areas.

    9.3  The terrestrial environment

         Cadmium is introduced into the terrestrial environment from
    mining, non-ferrous metal production, landfill sites and from the
    application of sewage sludge, phosphate fertilizers, and manure.
    Background concentrations of cadmium are in the range of 0.1 to 0.4
    mg/kg soil and can reach 4.5 mg/kg in volcanic soils. Levels up to 160
    mg/kg soil have been found close to metal processing sources.

         Reduced breakdown of leaf litter and recycling of nutrients has
    been attributed to metal pollution in the field. Cadmium appears to be
    the most potent metal at inhibiting litter degradation. The effect is
    thought to be due largely to reduced populations of microorganisms,
    which are responsible for the final stages of litter decomposition.

         Plants take up cadmium and can translocate and accumulate it.
    However, uptake from soil is limited. Where there is high-level
    exposure to cadmium (in the range of hundreds of mg/kg), growth
    reduction is the major effect. Plants exposed to cadmium in the field
    for long periods can develop tolerance to the metal. There is no
    evidence of adverse effects of cadmium on plant populations in the
    field.

         Terrestrial invertebrates vary considerably in their sensitivity
    to cadmium. Some species can take up and store cadmium to levels of up
    to 5000 mg/kg body weight without apparent ill effects, while others
    show population effects at levels of a few mg/kg soil. Populations of
    some terrestrial invertebrates could be adversely affected at levels
    of cadmium contamination seen in the field. Isopods and earthworms are
    useful biomonitors for cadmium contamination. Invertebrates with high
    body burdens may pose a threat to predators.

         Kidney damage was found in experimental birds fed 20 mg
    cadmium/kg diet for 12 weeks, but not at lower doses. Reproductive
    effects have been observed at 200 mg/kg diet. A dose of 4 mg/kg
    affected the behaviour of ducklings. No effects of cadmium have been
    seen in terrestrial birds sampled from the field, although the cadmium

    level in the brain, kidney, and liver of pigeons has proved to be a
    good indicator of urban cadmium contamination.

         Small mammals accumulate cadmium in the vicinity of mining spoil.
    The ionic balance was affected in voles exposed experimentally to a
    concentration of 10 mg/kg diet.

         Populations of terrestrial organisms may also develop tolerance
    to cadmium after long-term exposure.

    10.  RECOMMENDATIONS FOR PROTECTING THE ENVIRONMENT

         To eliminate environmental effects, emissions of cadmium from the
    following sources should be reduced as far as is practicable:

    *    smelters

    *    incinerators

    *    sewage sludge applied to the land

    *    phosphate fertilisers

    *    cadmium-containing manure

    11.  FURTHER RESEARCH

    a)   More study is needed to clarify the effects of cadmium on the
         decomposition process of plant debris. Effects on the degree of
         nutrient cycling and long-term plant growth and the exact nature
         of the inhibition of decomposition require further attention.

    b)   The adsorption of cadmium to soil and sediment requires further
         study and quantification of coefficients. Modelling of binding
         and distribution in the environment is needed.

    c)   Organisms that are particularly sensitive (i.e. indicator
         species) or that play a critical role in ecological systems
         should be identified and studied with regard to the effects of
         cadmium.

    d)   Studies are needed on the basic mechanisms by which cadmium
         interacts with physiological and biochemical processes in
         organisms and within individual cells.

         There is a need to take certain precautions in studies on
    cadmium. Firstly, the speciation of the metal should be considered in
    experimental design and procedures and a clear measure of the
    available cadmium should be reported. Secondly, studies of the uptake
    and movement between trophic levels should include the relationship
    between the non-nutrient cadmium and the nutrients calcium and zinc.

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    Appendix 1.  Global emissions of trace metals from natural sources (x 1000 tonnes/year) a
                                                                                                                                     
                             Arsenic     Cadmium     Copper      Mercury     Lead        Selenium    Zinc
                                                                                                                                     
    Wind-borne soil particles

         range               0.3-5.0     0.01-0.4    0.9-15      0-0.01      0.3-7.5     0.01-0.35   3.0-35
         median              2.6         0.21        8.0         0.05        3.9         0.18        19

    Sea salt spray

         range               0.19-3.1    0-0.11      0.23-6.9    0-0.04      0.02-2.8    0-1.1       0.02-0.86
         median              1.7         0.06        3.6         0.02        1.4         0.55        0.44

    Volcanoes

         range               0.15-7.5    0.14-1.5    0.9-18      0.03-2.0    0.54-6.0    0.10-1.8    0.31-19
         median              3.8         0.82        9.4         1.0         3.3         0.95        9.6

    Forest fires

         range               0-0.38      0-0.22      0.1-7.5     0-0.05      0.06-3.8    0-0.52      0.3-15
         median              0.19        0.11        3.8         0.02        1.9         0.26        7.6

    Biogenic continental particulates

         range               0.2-0.5     0-0.83      0.1-5.0     0-0.04      0.02-2.5    0-0.25      0.3-5.0
         median              0.26        0.15        2.6         0.02        1.3         1.12        2.6

    Biogenic continental volatiles

         range               0.03-2.5    0-0.8       0.01-0.62   0.02-1.2    0.01-0.38   0.15-5.0    0.02-5.0
         median              1.3         0.04        0.32        0.61        0.20        2.6         2.5

    Appendix 1 (contd).
                                                                                                                                     
                             Arsenic     Cadmium     Copper      Mercury     Lead        Selenium    Zinc
                                                                                                                                     
    Biogenic marine

         range               0.16-4.5    0-0.1       0.02-0.75   0.04-1.5    0.02-0.45   0.4-9.0     0.04-6.0
         median              2.3         0.05        0.39        0.77        0.24        4.7         3.0

    Total emission

         range               0.86-23     0.15-2.6    2.3-54      0.1-4.9     0.97-23     0.66-18     4.0-86
         median              12          1.3         28          2.5         12          9.3         45
                                                                                                                                     

     a From: Nriagu (1989)

    Appendix 2.  Natural and anthropogenic emissions of trace metals to the atmosphere in 1983 (x 1000 tonnes/year) a
                                                                                                                                     
    Trace metal         Anthropogenic source     Natural source           Total emission           Natural/total emissions
                                                                                                                                     
    Arsenic             19 (12-26)               12 (0.86-23)             31 (13-49)               0.39

    Cadmium             7.6 (3.1-12)             1.3 (0.15-2.6)           8.9 (3.2-15)             0.15

    Copper              35 (20-51)               28 (2.3-54)              63 (22-105)              0.44

    Mercury             3.6 (0.91-6.2)           2.5 (0.10-4.9)           6.1 (1.0-11)             0.41

    Lead                332 (289-376)            12 (0.97-23)             344 (290-399)            0.04

    Selenium            6.3 (3.0-9.7)            9.3 (0.66-18)            16 (2.5-24)              0.58

    Zinc                132 (70-194)             45 (4.0-86)              177 (74-280)             0.34
                                                                                                                                     

     a From: Nriagu (1989)

    Appendix 3.  Sources of global emissions of trace elements to the atmosphere in 1983 (tonnes/year) a
                                                                                                                                     
                  Arsenic          Cadmium          Copper           Mercury          Lead             Selenium         Zinc
                                                                                                                                     
    Coal combustion - electric utilities
                  232-1550         77-387           930-3100         155-542          775-4650         108-775          1085-7750

    Coal combustion - industry and domestic
                  198-1980         99-495           1390-4950        495-2970         990-9900         792-1980         1485-11 880

    Oil combustion - electric utilities
                  5.8-29           23-174           348-2230         -                232-1740         35-290           174-1280

    Oil combustion - industry and domestic
                  7.2-72           18-72            179-1070         -                716-2150         107-537          358-2506

    Pyrometallurgical non-ferrous metal production - mining
                  40.0-80          0.6-3            160-800          -                1700-3400        18-176           310-620

    Pyrometallurgical non-ferrous metal production - Pb production
                  780-1560         39-195           234-312          7.8-16           11 700-31 200    195-390          195-468

    Pyrometallurgical non-ferrous metal production - Cu-Ni production
                  8500-12 750      1700-3400        14 450-33 600    37-207           11 050-22 100    427-1280         4250-8500

    Pyrometallurgical non-ferrous metal production - Zn-Cd production
                  230-690          920-4600         230-690          -                5520-11 500      92-23            46 000-82 800

    Secondary non-ferrous metal production
                  -                2.3-3.6          55-165           -                90-1440          3.8-19           270-1440

    Steel and iron manufacturing
                  355-2480         28-284           142-2840         -                1065-14 200      0.8-2.2          7100-31 950

    Refuse incineration - municipal
                  154-392          56-1400          980-1960         140-2100         1400-2800        28-70            2800-8400

    Refuse incineration - sewage sludge
                  15-60            3-36             30-180           15-60            240-300          3-30             150-450

    Appendix 3 (contd).
                                                                                                                                     
                  Arsenic          Cadmium          Copper           Mercury          Lead             Selenium         Zinc
                                                                                                                                     
    Phosphate fertilizers
                  -                68-274           137-685          -                55-274           0.4-1.2          1370-6850

    Cement production
                  178-890          8.9-534          -                -                18-14 240        -                1780-17 800

    Wood combustion
                  60-300           60-180           600-1200         60-300           1200-3000        -                1200-6000

    Mobile sources (gasoline)
                  -                -                -                -                248 030          -                -

    Miscellaneous
                  1250-2800        -                -                -                3900-5100        -                1724-4783

    Total emissions - range
                  12 000-25 630    3100-12 040      19 860-50 870    910-6200         288 700-376 000  1810-5780        70 250-193 500

    Total emissions - median
                  18 820           7570             35 370           3560             332 350          3790b            131 880
                                                                                                                                     

     a From: Nriagu & Pacyna (1988)
     b This value applies to particulate selenium only. Since volatile selenium accounts for about
       40% of the selenium released, the total selenium emission is estimated to be 6300 tonnes per year.

    Appendix 4.  Anthropogenic inputs of trace elements to aquatic ecosystems (x 1000 tonnes/year) a
                                                                                                                                     
                  Arsenic          Cadmium          Copper           Mercury          Lead             Selenium         Zinc
                                                                                                                                     
    Atmospheric fallout
                  3.6-7.7          0.9-3.6          6.0-15           0.22-1.8         87-113           0.54-1.1         21-58

    Other industrial sources
                  8.4-62.3         1.2-13.4         29-75            0.08-7.0         10-67            9.5-70.9         56-317

    Total - range
                  12-70            2.1-17           35-90            0.3-8.8          97-180           10-72            77-375

    Total - median
                  41               9.4              62               4.6              138              41               226

    Atmospheric fallout/total anthropogenic inputs (%)
                  14               24               17               22               72               2                17
                                                                                                                                     

     a From: Nriagu & Pacyna (1988)

    Appendix 5.  Anthropogenic inputs of trace elements to soils (x 1000 tonnes/year) a
                                                                                                                                     
                  Arsenic          Cadmium          Copper           Mercury          Lead             Selenium         Zinc
                                                                                                                                     
    Atmospheric fallout
                  8.4-18           2.2-8.4          14-36            0.63-4.3         202-263          1.3-2.6          49-135

    Other industrial sources
                  43.6-94          3.4-29.6         527-1331         0.97-10.7        277-850          4.7-73.4         640-1919

    Total input - range b
                  52-112           5.6-38           541-1367         1.6-15           479-1113         6.0-76           689-2054

    Total input - median b
                  82               22               954              8.3              796              41               1372

    Atmospheric fallout/total anthropogenic inputs (%) b
                  16               24               3                30               29               5                7
                                                                                                                                     

     a From: Nriagu & Pacyna (1988)
     b These data do not include inputs from mine tailings, smelter slags and wastes to land.

    
    RESUME

         Le cadmium (numéro atomique 48; masse atomique relative 112,40)
    est un élément métallique qui appartient, avec le zinc et le mercure,
    au groupe IIb du tableau périodique. Certains sels de cadmium, tels
    que le sulfure, le carbonate et l'oxyde sont presque insolubles dans
    l'eau; ils peuvent cependant ętre transformés en sels solubles dans
    l'environnement naturel. La formation de différents dérivés du cadmium
    dans l'environnement est importante pour l'évaluation du risque.

         La teneur moyenne en cadmium de l'eau de mer est d'environ 0,1
    µg/litre ou moins. L'eau des cours d'eau contient du cadmium dissous
    ŕ des concentrations allant de < 1 ŕ 13,5 ng/litre. Dans les régions
    écartées et inhabitées, on observe en général des concentrations de
    cadmium dans l'air inférieures ŕ 1 ng/m3. Dans les régions oů l'on
    ne connaît pas de pollution, la concentration médiane en cadmium dans
    le sol se situerait entre 0,2 et 0,4 mg/kg. Toutefois, on rencontre
    occasionnellement des valeurs beaucoup plus élevées pouvant aller
    jusqu'ŕ 160 mg/kg de terre.

         Certains facteurs environnementaux influent sur la fixation, et
    par voie de conséquence, sur les effets toxiques du cadmium sur les
    organismes aquatiques. Une élévation de température augmente la
    fixation et l'effet toxique du cadmium qui sont en revanche réduits
    lorsque la salinité de l'eau ou sa dureté augmentent. Les organismes
    d'eau douce sont sensibles ŕ des concentrations plus faibles de
    cadmium que les organismes marins. Plus la teneur de l'eau en matičres
    organiques est élevée, plus la fixation et les effets toxiques du
    cadmium sont réduits car ces matičres se lient au cadmium et en
    réduisent la biodisponibilité. Toutefois, on est fondé ŕ croire que
    certains dérivés organiques pourraient avoir un effet inverse.

         Le cadmium s'accumule facilement dans de nombreux organismes, en
    particulier les microorganismes et les mollusques, pour lesquels le
    facteur de bioconcentration peut atteindre plusieurs milliers. Les
    invertébrés terricoles concentrent égale-ment assez fortement le
    cadmium. Pour la plupart des organismes, le facteur de concentration
    est faible ŕ modéré, généralement inférieur ŕ 100. Dans de nombreux
    tissus, le cadmium est lié aux protéines. On a isolé d'organismes
    exposés au cadmium, des pro-téines qui fixent spécifiquement les
    métaux lourds (métallothio-néines). Le cadmium se concentre
    préférentiellement dans les reins, les branchies et le foie (ou leurs
    équivalents). L'élimination du métal s'effectue probablement par le
    rein, encore que chez les crustacés, il puisse ętre éliminé en
    quantités notables en passant dans l'exosquelette. Chez les plantes,
    le cadmium se concentre principalement dans les racines et ŕ un
    moindre degré dans les feuilles.

         Le cadmium est toxique pour de nombreux microorganismes.
    Toutefois, la présence de sédiments et de fortes concentrations de
    sels ou de matičres organiques en solution réduit ces effets toxiques.
    Ces effets s'exercent principalement sur la croissance et la

    réplication. Parmi les microorganismes terricoles, les plus affectés
    sont les champignons, dont certaines espčces peuvent ętre éliminées
    lorsque le sol est contaminé par du cadmium. Une faible exposition au
    cadmium présent dans le sol peut entraîner une sélection des souches
    résistantes. La toxicité du cadmium pour les organismes aquatiques est
    variable, męme lorsqu'il s'agit d'espčces trčs proches et elle est
    liée ŕ la concentration du métal sous forme ionique. Le cadmium
    perturbe le métabolisme du calcium chez l'animal. Chez les poissons,
    il provoque une hypocalcémie, probablement en inhibant la fixation du
    calcium ŕ partir de l'eau. Toutefois, la présence de fortes
    concentrations de calcium dans l'eau protčge les poissons par
    inhibition compétitive de la fixation de cadmium. Le zinc accroît la
    toxicité du cadmium pour les invertébrés aquatiques. On a fait état
    d'effets sublétaux sur la croissance et la reproduction d'invertébrés
    aquatiques; des effets ont été également observés sur la structure des
    branchies d'invertébrés. Le cadmium est plus ou moins toxique pour les
    poissons, les salmonidés étant particuličrement sensibles. On a
    signalé des effets sublétaux chez les poissons, en particuliers des
    malformations de l'épine dorsale. Les stades les plus sensibles sont
    les embryons et les jeunes larves, les moins sensibles étant les
    oeufs. Chez les poissons, on n'observe pas d'interaction systématique
    entre le cadmium et le zinc. Le cadmium est toxique pour certaines
    larves d'amphibiens, mais on a constaté que la présence de sédiments
    dans les aquariums expérimentaux apportait une certaine protection.

         Le cadmium perturbe la croissance des végétaux au laboratoire,
    mais aucun effet n'a été observé dans la nature. Les plantes captent
    plus facilement le métal lorsqu'il est présent dans les solutions
    nutritives que lorsqu'il est dans le sol; les effets observés l'ont
    été essentiellement lors d'études portant sur des cultures
    hydroponiques. Il semblerait que le cadmium présent dans les solutions
    nutritives affecte l'ouverture des stomates, la transpiration et la
    photosynthčse.

         Les invertébrés terrestres sont relativement insensibles aux
    effets toxiques du cadmium, probablement ŕ cause de l'intervention de
    mécanismes de séquestration efficaces au niveau des divers organes.

         Les gastéropodes terrestres peuvent subir des effets sublétaux,
    principalement en ce qui concerne la consommation de nourriture et la
    dormance, mais uniquement ŕ des doses trčs élevées. Męme ŕ forte dose,
    le cadmium n'entraîne pas la mortalité des oiseaux mais peut provoquer
    des lésions rénales.

         Des études effectuées sur le terrain ont montré que le cadmium
    pouvait entraîner la modification de la proportion relative des
    diverses espčces dans les populations de microorganismes et de
    certains invertébrés aquatiques. La décomposition des feuilles mortes
    est fortement entravée par une forte pollution due aux métaux lourds,
    et le cadmium en serait le principal responsable.

    RESUMEN

         El cadmio (número atómico 48; masa atómica relativa 112,40) es un
    elemento metálico que pertenece, junto con el zinc y el mercurio, al
    grupo IIb de la tabla periódica. Algunas sales de cadmio, como el
    sulfuro, el carbonato y el óxido, son prácticamente insolubles en
    agua; pueden convertirse en sales hidrosolubles en el medio natural.
    El sulfato, el nitrato y los haluros son hidrosolubles. La especiación
    del cadmio en el medio ambiente tiene importancia para evaluar su
    potencial de riesgo.

         El contenido medio de cadmio en el agua de mar es de alrededor de
    0,1 µg/litro o menos. El agua de los ríos contiene cadmio disuelto en
    concentraciones que varían entre < 1 y 13,5 ng/litro. En zonas
    aisladas y deshabitadas, las concentraciones de cadmio en el aire
    suelen ser inferiores a 1 ng/m3. En zonas que se suponen no
    contaminadas, se ha comunicado que la concentración mediana de cadmio
    en el suelo se encuentra entre 0,2 y 0,4 mg/kg. No obstante, a veces
    se encuentran valores mucho más altos, que pueden llegar hasta 160
    mg/kg de suelo.

         Los factores ambientales influyen en la captación y, por ende, en
    los efectos tóxicos del cadmio en los organismos acuáticos. Al
    aumentar la temperatura aumentan la captación y los efectos tóxicos,
    mientras que el aumento de la salinidad o de la dureza del agua los
    hace disminuir. Los organismos de agua dulce sufren los efectos del
    cadmio en concentraciones inferiores a las que afectan a los
    organismos marinos. La materia orgánica contenida en el agua suele
    reducir la captación y los efectos tóxicos fijando el cadmio y
    reduciendo su disponibilidad para los seres vivos. Sin embargo, hay
    pruebas de que cierto tipo de materia orgánica puede ejercer el efecto
    contrario.

         El cadmio se acumula fácilmente en numerosos seres vivos,
    particularmente microorganismos y moluscos, en los que los factores de
    bioconcentración son del orden de varios millares. Los invertebrados
    del suelo también concentran este metal en grado considerable. La
    mayoría de los organismos presentan factores de concentración bajos o
    moderados (inferiores a 100). El cadmio está ligado a proteínas en
    numerosos tejidos. En organismos expuestos a ese metal se han aislado
    proteínas fijadoras de metales pesados (metalotioneínas). La
    concentración de cadmio es más elevada en el rińón, las branquias y el
    hígado (o sus equivalentes). La eliminación se produce probablemente
    por vía renal, si bien los crustáceos pueden eliminar cantidades
    importantes con la muda del exoesqueleto. En las plantas, el cadmio se
    concentra principalmente en las raíces y, en menor medida, en las
    hojas.

         El cadmio tiene efectos tóxicos para muy diversos
    microorganismos. No obstante, la presencia de sedimentos y las
    concentraciones elevadas de sales disueltas o materia orgánica reducen
    esos efectos. Los procesos más afectados son el crecimiento y la

    replicación. Los organismos del suelo más vulnerables son los hongos:
    algunas especies desaparecen tras la exposición al cadmio en el suelo.
    Tras exposiciones reducidas al metal en el suelo, se observa una
    selección a favor de las cepas resistentes.

         La toxicidad aguda del cadmio para los organismos acuáticos es
    variable, incluso entre especies estrechamente emparentadas, y guarda
    relación con la concentración de iones libres del metal. El cadmio
    interacciona con el metabolismo del calcio en los animales. En los
    peces provoca hipocalcemia, probablemente al inhibir la captación de
    calcio a partir del agua. No obstante, las concentraciones elevadas de
    calcio en el agua los protegen de la ingestión de cadmio por
    competencia en los lugares de captación. El zinc aumenta la toxicidad
    del cadmio para los invertebrados acuáticos. Se han notificado efectos
    subletales en el crecimiento y la reproducción de invertebrados
    acuáticos, así como modificaciones estructurales en las branquias de
    invertebrados. Hay pruebas de la selección de estirpes resistentes de
    invertebrados acuáticos tras la exposición al cadmio sobre el terreno.
    La toxicidad es variable en los peces; los salmónidos son
    especialmente susceptibles. Se han notificado efectos subletales en
    los peces, en particular malformaciones de la espina dorsal. Las fases
    biológicas más susceptibles son el embrión y la larva joven; los
    huevos son los menos vulnerables. No se ha observado una interacción
    homogénea entre el cadmio y el zinc en los peces. El cadmio resulta
    tóxico para algunas larvas de anfibios, si bien los sedimentos en el
    recipiente de ensayo confieren cierta protección.

         El cadmio afecta al crecimiento de las plantas en estudios
    experimentales, pero sobre el terreno no se ha observado efecto
    alguno. El metal es absorbido por las plantas con más rapidez a partir
    de soluciones de nutrientes que a partir del suelo; los efectos se han
    observado sobre todo en estudios de cultivo en soluciones de
    nutrientes. En éstas se ha notificado que el cadmio influye en la
    apertura de los estomas, la transpiración y la fotosíntesis.

         Los invertebrados terrestres son relativamente insensibles a los
    efectos tóxicos del cadmio, probablemente debido a la existencia de
    mecanismos eficaces de captura y fijación en ciertos órganos.

         Los gasterópodos terrestres sufren efectos subletales; los
    principales procesos afectados son el consumo de alimentos y el
    letargo, pero sólo con dosis muy elevadas. El metal no produce efectos
    letales en las aves, ni siquiera con dosis elevadas, si bien se
    observan lesiones renales.

         En estudios de campo se ha comunicado que el cadmio induce
    cambios en la composición de especies en las poblaciones de
    microorganismos y ciertos invertebrados acuáticos. La descomposición
    del mantillo de hojas se ve notablemente reducida por la contaminación
    con metales pesados; se ha identificado al cadmio como el principal
    causante de este efecto.



    See Also:
       Toxicological Abbreviations