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BIOAVAILABILITY OF HEAVY METALS IN SEDIMENT
OF SHALLOW MARINE ECOSYSTEM
BY
C.U.EBONG
SUMMARY
The pollution of marine ecosystems by heavy metals is a worldwide problem and
the situation is aggravated by the ability of these ecosystems to concentrate and
accumulate some metals within food chains. Marine organisms, particularly filter
feeders, can take up these metals through their digestive systems, thus increasing
the potential for their entry into the human food chain . Heavy metals are among
the most serious pollutants of great environmental concern because they are
nondegradable, toxic and persistent with serious ecological consequences
especially on aquatic ecosystem. The marine ecosystems are strongly influenced by
long term discharge of untreated domestic and industrial wastewaters, storm water
runoff, accidental spills and direct solid waste dumping.
Keywords: Bioavailability, Heavy metals in sediment, shallow Marine ecosystem.
TABLE OF CONTENTS
Title Page
Summary
Introduction
Heavy Metals
Bioavailability of Heavy Metals in Marine Organisms
Entry Mode
Effect of Heavy Metals on Marine Organism
Conclusion
INTRODUCTION
Bioavailability is the extent to which a toxic contaminant is present in a form or
species which will be available for biologically mediated transformations in an
aquatic environment (Horsfall, 2011).
Bioavailability of heavy metals in marine ecosystem refers to the amount of heavy
metals that becomes available (reaches the target organ or systemiccirculation) to
an aquatic organism's body when introduced through ingestion, inhalation,
injection, or skincontact.
The pollution of marine ecosystems by heavy metals is a worldwide problem
(Bryan, 1976), and the situation is aggravated by the ability of these ecosystems to
concentrate and accumulate some metals within food chains.
The current alarm about metal pollution in the sea however started with the
tragedy of disease caused by the consumption of mercury and lead contaminated
fish from marine ecosystem.
Humans have always depended on aquatic resources for food and medicines as
well as recreational and commercial purposes such as fishing and tourism. In
addition, marine ecosystems have significant impact on migratory bird species that
use the water bodies and surroundings as sanctuary, stop-over for food, breeding
and nesting.
HEAVY METALS
Heavy metals are metals and metalloids which are stable and have density greater
than 5g/cm3.The term originated with reference to the harmful effects of cadmium,
mercury and lead, all of which are denser than iron. It includes transition metals
like chromium, cobalt, nickel, copper, zinc, cadmium, mercury, lead, arsenic,
antimony and bismuth. Of these, the most toxic metallic pollutants are mercury,
lead, zinc and copper. Heavy metals occur naturally in the marine environment. In
addition, these heavy metals enter the aquatic systems by direct discharges via
industrial and urban effiuents, surface run off and indirectly from aerial fallout.
The use of heavy metal fungicides in agriculture is increasing as seed-dressing
agents. Antifouling properties of mercury compounds are yet used in pulp mills,
industrial and domestic sewage wastes from various sources are now a threat to
the survival of fishes and other organisms.
Certain metals are essential to normal growth and development of organisms, but
some are toxic. An element can be regarded as essential only;
i. If the organism can neither grow nor complete its life cycle in the absence
of the element.
ii. If the element cannot be replaced by any other element, and;
iii. If the element exerts a direct influence on organism and its metabolism.
Similarly, an element can be regarded as toxic if that element injures growth or
metabolism of an organism when supplied above a certajn concentration. In fact,
all metals are toxic at high concentrations but"some are highly toxic even at lower
concentrations. Elements like copper, mercury, lead, cadmium, zinc and
chromium are very toxic. Except copper and zinc, others are non-.essential.
CONCENTRATION OF HEAVY METALS IN MARINE ORGANISMS
Because certain metals are required in life processes, most organisms have a
capability of concentrating them. Capability is enhanced by some feeding and
metabolic processes which can lead to enormously high concentrations.
Invertebrates appear to have a particularly high capability for concentrating
metals along with other foreign materials found in their environment when they
filter plankton during feeding. Fishes apparently can accumulate metals either
directly from sea water or indirectly through food chain.
Because of the ability of many metals to form complexes with organic substances,
they have a tendency to be fixed in the tissue and not to be excreted. In other
words, they have a large biological half-time. This is perhaps one of the major
problems that metals has with respect to their effects on aquatic organisms.
Many marine fishes and shell fish have got the capacity to concentrate trace
metals in their tissues to much higher levels than they are in other organisms and
also they concentrate them several hundred times more than the concentration of
metals in sea water. Bioassay studies are also required on food organisms of
commercially valuable species.
If concentrations of metals are not high enough to kill the fish, but are high
enough to destroy the organisms on which the fish feeds, there will be
substantial damage to fishery.
BIOAVAILABILITY OF HEAVY METAL IN MARINE ORGANISM
At sufficiently high concentrations, heavy metals are toxic to marine organisms
and to their consumers at higher trophic levels including man. Toxicity of a
metal and its effects on organisms depends on:
i. The chemical form of metal (exchangeable fraction, bound to carbonates,
bound to oxides, bound to organics, residual or inert fraction).
ii. Presence of other metals
iii. Physiological status of organisms, and;
iv. Environmental physico-chemical parameters like salinity, temperature,
dissolved oxygen and the pH of water.
In general, metals are less toxic at lower temperatures and high salinity than at
high temperatures and lower salinity. Toxicity of a metal is also dependent upon
residence time of metals concerned. Generally, most metals have a long residence
time and hence exert their toxic effect over a long time.
The oceans provide a vital sink for many heavy metals and their compounds. There
is a growing concern that the natural cycling rates of many metals are being
disturbed by anthropogenic activities, especially the release from industrial,
domestic and urban effluents of increasing amounts of Pb, Zn, Cd, Hg and Cu.32
Mercury is a typical example of metal pollution from natural and anthropogenic
activities. It is estimated that up to 150.000 tones of Hg are released as a result of
degassing from the Earth’s crust and 8.000-10.000 tones from industrial and urban
activities.
Lead (Pb) is another typical example of anthropogenic metal pollution. Beginning
with very low levels at about 2.700 years ago, Pb concentration increased during
the industrial age and has risen rapidly since Pb was added to gasoline fuel of
vehicles. Pb levels in Greenland ice have risen 200-fold from the natural level.
Atmospheric metal pollution is responsible from most of the dissolved Cd, Cu, Fe,
Zn, Ni and As in the oceans.
High levels of heavy metals have been found in sediment and biota of marine
environment. As a consequence there is an increase in the bioavailability of many
heavy metals to marine biota.
ENTRY MODE
It has been known for many years that concentration of heavy metals is
significantly higher in marine biosphere. Today, additional quantities of heavy
metals are being added to marine ecosystem from agricultural and industrial
waters, hospitals, domestic sewage and from the polluted atmosphere.
Entry of heavy metals into organisms depends upon the rate of absorption of a
metal by animals which is affected by factors like salinity, pH , presence of other
metals, complexing agents, temperature, size difference, maturity and starvation
of the animal.
Some metals enter the marine ecosystem from the atmosphere, e.g. natural inputs
of metals, such as Aluminium (Al) in wind-blowing dust of rocks and shales, and
mercury (Hg) from volcanic activity. Lead (Pb) inputs in the atmosphere from
industrial and vehicular exhaust are much greater than natural inputs. Some metals
are deposited by gas exchange at the sea surface, by fallout of particles (dry
deposition) or are scavenged from the air column by precipitation (rain) which is
called wet deposition
Most metallic elements occur naturally in marine environments, and are
classified as pollutants only when added by man in quantities sufficient to
produce deleterious effects.
In the natural environment, organisms are exposed chronically to sublethal
concentrations of several contaminants simultaneously, and concentrations of
metals present within the organisms result from the relative rates of metal
accumulation and turnover. These rates vary among species and also with the
concentration apd physicochemical form of the metal. Assessment of potential
effects of metal contaminants on marine organisms must consider organismic
response not only to levels of metals in the environment, but also the contained
metals. Furthermore, both the cycling of a particular metal and its toxicity
characteristics may depend upon the physicochemical form of the metal
introduced into the system. An understanding of the potential physiological
effects resulting from contaminative metal additions to marine environments
therefore requires knowledge of the complex physical and biological processes
that control distribution and turn over of metals in the component organisms and
in the entire ecosystem. With the growing interest in pollution of marine
environment, many countries are conducting monitoring studies on metals in
both seawater and marine organisms. Invertebrates are considered excellent
indicator organisms because of their ability in concentrating metals, among
other pollutants. Besides measuring concentrations of these metals in aquatic
organisms, there is a need to study effects of concentrated metals on organisms
and on ecosystem. This will require careful evaluation of effects of metals on
various trophic levels in marine ecosystem and movement of metals through
food web.
EFFECT OF HEAVY METALS ON MARINE ORGANISM
The effects of heavy metals on aquatic organisms can be divided into:
a. Direct effects and;
b. Indirect eftects.
The direct effects are seen in behaviour, migration, physiology, metabolism,
reproduction, development and growth of aquatic animals.
The indirect effect is effected through the effect on food chain organisms and
ecological stress.
CONCLUSION
The real problem today is not whether heavy metalsin marine ecosystems are
toxic or not, but what concentrations are permissible and safe in our aquatic
environment and do not produce harmful effects on users of water and fish from
the waters. Although much work has been done on heavy metal pollutants, there
is still a great need for information on normal responses and functions of
organisms, to assess influences of metals and their toxicities fully. It is impossible
to prevent pollution of marine environment totally but awareness must be created
on metal pollution. Pollution of marine ecosystem could be minimized by certain
precautionary measures like development of adequate environmental control
and management. Continuous monitoring of our environment and food products
from these waters must be built up.
REFERENCES
Clark RB, Frid C, Attrill M. Marine Pollution, 4th edit. Oxford University Press,
Oxford, 1997, Chapter Metals, pp.61-79.
Nieboer E, Richardson DHS. The replacement of the nondescript term “heavy
metals” by the biologically and chemically significant classification of metal
ions.Environ Pollut B1:3-26, 1980. 1980.
Phillips DJH. The chemistries and environmental fates of trace metals and
organochlorines in aquatic ecosystems. Mar Pollut Bull 31:193-200, 1995.
Depledge MH, Weeks JM, Bierregaard P. Heavy metals. In: Callow P (Ed.).
Handbook of Ecotoxicology. Blackwell Science, Oxford, 1998, pp. 543-569.
Forster U, Whittmann GTW. Metal Pollution in the Aquatic Environment.
Springer-Verlag, Berlin, 1983.
Meria E, (Ed). Metals and Their Compounds in the Environment. Occurrence,
Analysis and Biological Relevance. Verlag Chemie, New York, 1991.
Market B, Friese K (Eds). Trace Elements. Their Distribution and Effects in the
Environment. Elsevier, Amsterdam, 2000.
Newman MC, McIntosh AW (Eds), Metal Ecotoxicology, Concepts and
Applications.Lewis, Boca Raton, FL, 1990.
Dallinger E, Rainbow PS. Ecotoxicology of Metals in Invertebrates. Lewis, Boca
Raton, FL, 1992.
Nriagu JO (Ed.). The Biogeochemistry of Lead in the Environment. Part A.
Ecological Cycles, Part B. Biological Effects. Elsevier/North Holland
BiomedicalPress, Amsterdam, 1978.
Nriagu JO (Ed.). Copper in the Environment. Parts 1 and 2. Wiley Interscience,
Chichester, UK, 1979.
Nriagu JO (Ed.). Zinc in the Environment, Parts 1 and 2. Wiley Interscience,
Chichester, UK, 1980.
Nriagu JO (Ed.). Cadmium in the Environment Part 1. Wiley Interscience,
Chichester, UK, 1980.
Nriagu JO, Nieber E (Eds.). Chromium in the Natural and Human Environment.
Wiley & Sons, New York, 1987.
Nriagu JO (Ed.). Arsenic in the Environment. Part II. Human Health and
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Chapman PM, Allen HE, Z’Graggen MN. Evaluation of bioaccumulation factors in
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Rand GM, Petrocelli SR (Eds). Fundamentalsof Aquatic Toxicology. Methods and
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Regan L. The design of metal-binding in proteins. Review. Annu Rev Biophys.
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toxicity. Review. Environ Int 33: 576-582, 2007.
Malins DC, Ostrander GK (Eds.). Aquatic Toxicology-Molecular, Biochemical and
Cellular Perspectives. Lewis, Boca Raton, FL, 1993, pp. 387-420.
Reidel GF, Abbe GR, Sanders JG. Silver and copper accumulation in two estuarine
ffbivalves, the eastern oyster (Crassostrea virginica) and the hooked mussel
(Ischadium rearrum). Estuaries 18:445-455, 1995.
Bryan GW. Concentration of zinc and copperin the tissues of decapod crustaceans.
J Mar Biol Assoc UK 48:303-321, 1968.
Bryan GW, Langston WJ. Bioavailability, accumulation and effects of heavy
metalsin sediments with special reference to United Kingdom estuaries: a
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Lewis AG, Cave WR. The biological importance of copperin oceans and estuaries.
Oceanogr Mar Biol Annu Rev 20:471-495, 1982.
Bryan GW. The effect of heavy metals (other than mercury) on marine and
estuarine organisms. Progr R Soc London Ser B 177:389-410, 1971.
McKenna JM, Chaney RL, Williams FM. The effect of cadmium and zinc
interactionson the accumulation and tissue distribution of zinc and cadmium
in lettuce andspinach. Environ Pollut 79:113-120, 1993.
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Toxicology 127:55-62, 2002.
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Publications,Oxford, 1990.

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Bioavailability of heavy metals in sediment C.U.EBONG

  • 1. BIOAVAILABILITY OF HEAVY METALS IN SEDIMENT OF SHALLOW MARINE ECOSYSTEM BY C.U.EBONG SUMMARY The pollution of marine ecosystems by heavy metals is a worldwide problem and the situation is aggravated by the ability of these ecosystems to concentrate and accumulate some metals within food chains. Marine organisms, particularly filter feeders, can take up these metals through their digestive systems, thus increasing the potential for their entry into the human food chain . Heavy metals are among the most serious pollutants of great environmental concern because they are nondegradable, toxic and persistent with serious ecological consequences especially on aquatic ecosystem. The marine ecosystems are strongly influenced by long term discharge of untreated domestic and industrial wastewaters, storm water runoff, accidental spills and direct solid waste dumping. Keywords: Bioavailability, Heavy metals in sediment, shallow Marine ecosystem. TABLE OF CONTENTS
  • 2. Title Page Summary Introduction Heavy Metals Bioavailability of Heavy Metals in Marine Organisms Entry Mode Effect of Heavy Metals on Marine Organism Conclusion
  • 3. INTRODUCTION Bioavailability is the extent to which a toxic contaminant is present in a form or species which will be available for biologically mediated transformations in an aquatic environment (Horsfall, 2011). Bioavailability of heavy metals in marine ecosystem refers to the amount of heavy metals that becomes available (reaches the target organ or systemiccirculation) to an aquatic organism's body when introduced through ingestion, inhalation, injection, or skincontact. The pollution of marine ecosystems by heavy metals is a worldwide problem (Bryan, 1976), and the situation is aggravated by the ability of these ecosystems to concentrate and accumulate some metals within food chains. The current alarm about metal pollution in the sea however started with the tragedy of disease caused by the consumption of mercury and lead contaminated fish from marine ecosystem. Humans have always depended on aquatic resources for food and medicines as well as recreational and commercial purposes such as fishing and tourism. In addition, marine ecosystems have significant impact on migratory bird species that use the water bodies and surroundings as sanctuary, stop-over for food, breeding and nesting. HEAVY METALS Heavy metals are metals and metalloids which are stable and have density greater than 5g/cm3.The term originated with reference to the harmful effects of cadmium, mercury and lead, all of which are denser than iron. It includes transition metals like chromium, cobalt, nickel, copper, zinc, cadmium, mercury, lead, arsenic, antimony and bismuth. Of these, the most toxic metallic pollutants are mercury,
  • 4. lead, zinc and copper. Heavy metals occur naturally in the marine environment. In addition, these heavy metals enter the aquatic systems by direct discharges via industrial and urban effiuents, surface run off and indirectly from aerial fallout. The use of heavy metal fungicides in agriculture is increasing as seed-dressing agents. Antifouling properties of mercury compounds are yet used in pulp mills, industrial and domestic sewage wastes from various sources are now a threat to the survival of fishes and other organisms. Certain metals are essential to normal growth and development of organisms, but some are toxic. An element can be regarded as essential only; i. If the organism can neither grow nor complete its life cycle in the absence of the element. ii. If the element cannot be replaced by any other element, and; iii. If the element exerts a direct influence on organism and its metabolism. Similarly, an element can be regarded as toxic if that element injures growth or metabolism of an organism when supplied above a certajn concentration. In fact, all metals are toxic at high concentrations but"some are highly toxic even at lower concentrations. Elements like copper, mercury, lead, cadmium, zinc and chromium are very toxic. Except copper and zinc, others are non-.essential. CONCENTRATION OF HEAVY METALS IN MARINE ORGANISMS Because certain metals are required in life processes, most organisms have a capability of concentrating them. Capability is enhanced by some feeding and metabolic processes which can lead to enormously high concentrations. Invertebrates appear to have a particularly high capability for concentrating metals along with other foreign materials found in their environment when they
  • 5. filter plankton during feeding. Fishes apparently can accumulate metals either directly from sea water or indirectly through food chain. Because of the ability of many metals to form complexes with organic substances, they have a tendency to be fixed in the tissue and not to be excreted. In other words, they have a large biological half-time. This is perhaps one of the major problems that metals has with respect to their effects on aquatic organisms. Many marine fishes and shell fish have got the capacity to concentrate trace metals in their tissues to much higher levels than they are in other organisms and also they concentrate them several hundred times more than the concentration of metals in sea water. Bioassay studies are also required on food organisms of commercially valuable species. If concentrations of metals are not high enough to kill the fish, but are high enough to destroy the organisms on which the fish feeds, there will be substantial damage to fishery. BIOAVAILABILITY OF HEAVY METAL IN MARINE ORGANISM At sufficiently high concentrations, heavy metals are toxic to marine organisms and to their consumers at higher trophic levels including man. Toxicity of a metal and its effects on organisms depends on: i. The chemical form of metal (exchangeable fraction, bound to carbonates, bound to oxides, bound to organics, residual or inert fraction). ii. Presence of other metals iii. Physiological status of organisms, and; iv. Environmental physico-chemical parameters like salinity, temperature, dissolved oxygen and the pH of water.
  • 6. In general, metals are less toxic at lower temperatures and high salinity than at high temperatures and lower salinity. Toxicity of a metal is also dependent upon residence time of metals concerned. Generally, most metals have a long residence time and hence exert their toxic effect over a long time. The oceans provide a vital sink for many heavy metals and their compounds. There is a growing concern that the natural cycling rates of many metals are being disturbed by anthropogenic activities, especially the release from industrial, domestic and urban effluents of increasing amounts of Pb, Zn, Cd, Hg and Cu.32 Mercury is a typical example of metal pollution from natural and anthropogenic activities. It is estimated that up to 150.000 tones of Hg are released as a result of degassing from the Earth’s crust and 8.000-10.000 tones from industrial and urban activities. Lead (Pb) is another typical example of anthropogenic metal pollution. Beginning with very low levels at about 2.700 years ago, Pb concentration increased during the industrial age and has risen rapidly since Pb was added to gasoline fuel of vehicles. Pb levels in Greenland ice have risen 200-fold from the natural level. Atmospheric metal pollution is responsible from most of the dissolved Cd, Cu, Fe, Zn, Ni and As in the oceans. High levels of heavy metals have been found in sediment and biota of marine environment. As a consequence there is an increase in the bioavailability of many heavy metals to marine biota. ENTRY MODE It has been known for many years that concentration of heavy metals is significantly higher in marine biosphere. Today, additional quantities of heavy metals are being added to marine ecosystem from agricultural and industrial waters, hospitals, domestic sewage and from the polluted atmosphere.
  • 7. Entry of heavy metals into organisms depends upon the rate of absorption of a metal by animals which is affected by factors like salinity, pH , presence of other metals, complexing agents, temperature, size difference, maturity and starvation of the animal. Some metals enter the marine ecosystem from the atmosphere, e.g. natural inputs of metals, such as Aluminium (Al) in wind-blowing dust of rocks and shales, and mercury (Hg) from volcanic activity. Lead (Pb) inputs in the atmosphere from industrial and vehicular exhaust are much greater than natural inputs. Some metals are deposited by gas exchange at the sea surface, by fallout of particles (dry deposition) or are scavenged from the air column by precipitation (rain) which is called wet deposition
  • 8. Most metallic elements occur naturally in marine environments, and are classified as pollutants only when added by man in quantities sufficient to produce deleterious effects. In the natural environment, organisms are exposed chronically to sublethal concentrations of several contaminants simultaneously, and concentrations of metals present within the organisms result from the relative rates of metal accumulation and turnover. These rates vary among species and also with the concentration apd physicochemical form of the metal. Assessment of potential effects of metal contaminants on marine organisms must consider organismic response not only to levels of metals in the environment, but also the contained metals. Furthermore, both the cycling of a particular metal and its toxicity characteristics may depend upon the physicochemical form of the metal introduced into the system. An understanding of the potential physiological effects resulting from contaminative metal additions to marine environments therefore requires knowledge of the complex physical and biological processes that control distribution and turn over of metals in the component organisms and in the entire ecosystem. With the growing interest in pollution of marine environment, many countries are conducting monitoring studies on metals in both seawater and marine organisms. Invertebrates are considered excellent indicator organisms because of their ability in concentrating metals, among other pollutants. Besides measuring concentrations of these metals in aquatic organisms, there is a need to study effects of concentrated metals on organisms and on ecosystem. This will require careful evaluation of effects of metals on various trophic levels in marine ecosystem and movement of metals through food web.
  • 9. EFFECT OF HEAVY METALS ON MARINE ORGANISM The effects of heavy metals on aquatic organisms can be divided into: a. Direct effects and; b. Indirect eftects. The direct effects are seen in behaviour, migration, physiology, metabolism, reproduction, development and growth of aquatic animals. The indirect effect is effected through the effect on food chain organisms and ecological stress. CONCLUSION The real problem today is not whether heavy metalsin marine ecosystems are toxic or not, but what concentrations are permissible and safe in our aquatic environment and do not produce harmful effects on users of water and fish from the waters. Although much work has been done on heavy metal pollutants, there is still a great need for information on normal responses and functions of organisms, to assess influences of metals and their toxicities fully. It is impossible to prevent pollution of marine environment totally but awareness must be created on metal pollution. Pollution of marine ecosystem could be minimized by certain precautionary measures like development of adequate environmental control and management. Continuous monitoring of our environment and food products from these waters must be built up.
  • 10. REFERENCES Clark RB, Frid C, Attrill M. Marine Pollution, 4th edit. Oxford University Press, Oxford, 1997, Chapter Metals, pp.61-79. Nieboer E, Richardson DHS. The replacement of the nondescript term “heavy metals” by the biologically and chemically significant classification of metal ions.Environ Pollut B1:3-26, 1980. 1980. Phillips DJH. The chemistries and environmental fates of trace metals and organochlorines in aquatic ecosystems. Mar Pollut Bull 31:193-200, 1995. Depledge MH, Weeks JM, Bierregaard P. Heavy metals. In: Callow P (Ed.). Handbook of Ecotoxicology. Blackwell Science, Oxford, 1998, pp. 543-569. Forster U, Whittmann GTW. Metal Pollution in the Aquatic Environment. Springer-Verlag, Berlin, 1983. Meria E, (Ed). Metals and Their Compounds in the Environment. Occurrence, Analysis and Biological Relevance. Verlag Chemie, New York, 1991. Market B, Friese K (Eds). Trace Elements. Their Distribution and Effects in the Environment. Elsevier, Amsterdam, 2000. Newman MC, McIntosh AW (Eds), Metal Ecotoxicology, Concepts and Applications.Lewis, Boca Raton, FL, 1990.
  • 11. Dallinger E, Rainbow PS. Ecotoxicology of Metals in Invertebrates. Lewis, Boca Raton, FL, 1992. Nriagu JO (Ed.). The Biogeochemistry of Lead in the Environment. Part A. Ecological Cycles, Part B. Biological Effects. Elsevier/North Holland BiomedicalPress, Amsterdam, 1978. Nriagu JO (Ed.). Copper in the Environment. Parts 1 and 2. Wiley Interscience, Chichester, UK, 1979. Nriagu JO (Ed.). Zinc in the Environment, Parts 1 and 2. Wiley Interscience, Chichester, UK, 1980. Nriagu JO (Ed.). Cadmium in the Environment Part 1. Wiley Interscience, Chichester, UK, 1980. Nriagu JO, Nieber E (Eds.). Chromium in the Natural and Human Environment. Wiley & Sons, New York, 1987. Nriagu JO (Ed.). Arsenic in the Environment. Part II. Human Health and EcosystemEffect. Wiley Interscience, New York, 1994. Chapman PM, Allen HE, Z’Graggen MN. Evaluation of bioaccumulation factors in regulating metals. Environ Sci Technol 30(10) : 448A-452A, 1996. Rand GM, Petrocelli SR (Eds). Fundamentalsof Aquatic Toxicology. Methods and Applications. Hemisphere, New York, 1985, pp. 374-415. Regan L. The design of metal-binding in proteins. Review. Annu Rev Biophys. Biomol. Structure 22:257-281, 1993. Rainbow PS. Trace metal bioaccumulation: Models, metabolic availability and toxicity. Review. Environ Int 33: 576-582, 2007. Malins DC, Ostrander GK (Eds.). Aquatic Toxicology-Molecular, Biochemical and Cellular Perspectives. Lewis, Boca Raton, FL, 1993, pp. 387-420. Reidel GF, Abbe GR, Sanders JG. Silver and copper accumulation in two estuarine
  • 12. ffbivalves, the eastern oyster (Crassostrea virginica) and the hooked mussel (Ischadium rearrum). Estuaries 18:445-455, 1995. Bryan GW. Concentration of zinc and copperin the tissues of decapod crustaceans. J Mar Biol Assoc UK 48:303-321, 1968. Bryan GW, Langston WJ. Bioavailability, accumulation and effects of heavy metalsin sediments with special reference to United Kingdom estuaries: a review. Environ. Pollut 76:89-131, 1991. Lewis AG, Cave WR. The biological importance of copperin oceans and estuaries. Oceanogr Mar Biol Annu Rev 20:471-495, 1982. Bryan GW. The effect of heavy metals (other than mercury) on marine and estuarine organisms. Progr R Soc London Ser B 177:389-410, 1971. McKenna JM, Chaney RL, Williams FM. The effect of cadmium and zinc interactionson the accumulation and tissue distribution of zinc and cadmium in lettuce andspinach. Environ Pollut 79:113-120, 1993. Chang L, Magos L, Suzuki T (Eds.). Toxicology of Metals. CRC Press, Boca Raton, FL,1996. Bal W, Kasprzak KS. Induction of oxidative DNA damage by carcinogenic metals. Toxicology 127:55-62, 2002. UNEP. A review and the prospects for open ocean pollution monitoring. Internal report prepared for the Regional Seas Programme Activity Centre. UNEP- Monitoringand Assessment Research Centre, University of London, 1983. GESAMP. The State of the Marine Environment. Blackwell Scientific Publications,Oxford, 1990.