U.S DEPARTMENT OF COMMERCE
K jonal Technical I'' --mation Service
PB-290 659
Metal Bioaccumulation in
Fishes and Aquatic Invertebrates
A Literature Review
MontB"" State Univ, Bozeman Fisheries Bioassay Lab
Prepared for
Environmental Research Lab -Dulufh, MN
Dec 78
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RESEARCH REPORTING SERIES
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United
Environmental Protection
Ajpncy
Laboratory
Duluth MN 55804
... \ tO J ' ' • , v '
December 1978
Roccrrcrt end Development
290659
o a
on
Fishes and
A Literature Review
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TECHNICAL REPORT DATA
(Please read Instructions on the reverse before completing}
1. REPORT NO.
EPA-600/3-78-103
2.
4. TITLE AND SUBTITLE
Metal Bioaccumulation in Fishes and Aquatic
Invertebrates: A Literature Review
5. REPORT DATE
December 1978 issuing date
6. PERFORMING ORGANIZATION CODE'
3. R
7. AUTHOR(S)
Glenn R. Phillips and Rosemarie C. Russo
8. PERFORMING ORGANIZATION REPORT No"
9. PERFORMING ORGANIZATION NAME AND ADDRESS
Fisheries Bioassay Laboratory
Montana State University
Bozeman, Montana 59717
10, PROGRAM ELEMENT NO.
11. CONTRACT/GRANT NO.
R803950
12. SPONSORING AGENCY NAME AND ADDRESS
Environmental Research Laboratory—Duluth, MN
Office of Research and Development
U.S. Environmental Protection Agency
Duluth, Minnesota 55804
13. TYPE OF REPORT AND PERIOD COVERED
Final
14. SPONSORING AGENCY CODE
EPA/600/03
15. SUPPLEMENTARY NOTES
16. ABSTRACT
Literature concerning the bioaccumulation of metals by freshwater and marine
fishes and invertebrates has been reviewed; metal residue levels are also reported
for a few mammals and plants. Twenty-one metals are considered in individual sections
of the review and a bibliography of over 300 literature citations is included.
The major sources of each metal to the environment are listed as are the causes
and symptoms of metal toxicity in humans. Some discussion is included on the health
implications of human consumption of metal-contaminated aquatic organisms. Available
information is presented on: routes of accumulation, kinetics of accumulation and ex-
cretion, distribution within organisms, physiological responses of organisms, residue-
toxicity thresholds, chemical speciation relative to biological availability, and
microbial and chemical interconversions in aqueous systems. Major areas of insuf-
ficient knowledge are identified.
Few metals accumulate in the edible portions of aquatic organisms; moreover,
most metals when ingested orally have a relatively low toxicity to humans. However,
mercury, arsenic, and radioactive cesium may reach hazardous concentrations in edible
tissues of fishes and shellfishes; additionally, in shellfishes, cadmium, lead, and
other metal isotopes may exceed levels safe for human consumption.
17.
KEY WORDS AND DOCUMENT ANALYSIS
DESCRIPTORS
b.lDENTIFIERS/OPEN ENDED TERMS
c. COSATl Field/Group
Pollution
Residues
Metals
Aquatic organisms
Energy development
Metal bibliography
Bioaccumulation
Bi concentration
Heavy metals
06/F.T
18. DISTRIBUTION STATEMENT
RELEASE TO PUBLIC
19. SECURITY CLASS (ThisReport/
UNCLASSIFIED
20. SECURITY CLASS (This pagej
UNCLASSIFIED
22. PRICE
EPA Form 2220—1 (Rev. 4-77) PREVIOUS EDITION is OBSOLETE
U. S. GOVERNMENT PRINTING OFFICE: 1978 — 657-060/1559
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EPA-600/3-78-103
December 1978
METAL BIOACCUMULATION IN FISHES AND AQUATIC INVERTEBRATES:
A Literature Review
by
Glenn R. Phillips and Rosemarie C. Russo
Fisheries Bioassay Laboratory
Montana State University
Bozeman, Montana 59717
Grant No. R803950
Project Officer
Donald I. Mount
Environmental Research Laboratory
Duluth, Minnesota 55804
ENVIRONMENTAL RESEARCH LABORATORY
OFFICE OF RESEARCH AND DEVELOPMENT
U.S. ENVIRONMENTAL PROTECTION AGENCY
DULUTH, MINNESOTA 55804
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DISCLAIMER
This report has been reviewed by the Environmental Research Laboratory-
Duluth, U.S. Environmental Protection Agency, and approved for publication.
Approval does not signify that the contents necessarily reflect the views and
policies of the U.S. Environmental Protection Agency, nor does mention of trade
names or commercial products constitute endorsement or recommendation for use.
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FOREWORD
Residues of pollutants in aquatic organisms eaten by man have been the
object of concern in recent years. Several metals, notably mercury and
cadmium, have been involved in many places.
This report summarizes the literature on the bioaccumulation of heavy
metals in aquatic organisms. Since environmental release of metals from
energy development activities has been of much concern, this report should
be useful as a summary of the current state of knowledte on metal bioaccumu-
lation.
Donald I. Mount, Ph.D.
Director
Environmental Research Laboratory-Duluth
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ABSTRACT
Much of the available literature concerning the bioaccumulation of
metals by freshwater and marine fishes and invertebrates has been reviewed;
this includes literature reports of both laboratory and field investigations.
Metal residue levels are also reported for a few mammals and plants.
Twenty-one metals are considered in individual sections of this review and
a bibliography of over 300 literature citations is included.
The major sources of each metal to the environment are listed as are
the causes and symptoms of metal toxicity in humans. Some discussion is
included on the health implications of human consumption of metal-contaminatec
aquatic organisms. If data were available for particular metals, information
is presented on: routes of accumulation, kinetics of accumulation and ex-
cretion, distribution within organisms, physiological responses of organisms,.
residue-toxicity thresholds, chemical speciation relative to biological
availability, and microbial and chemical interconversions in aqueous systems.
Few metals accumulate in the edible portions of aquatic organisms;
moreover, most metals when ingested orally have a relatively low toxicity
to humans. However, mercury, arsenic, and radioactive cesium may reach
hazardous concentrations in edible tissues of fishes and shellfishes;
additionally, in shellfishes, cadmium, lead, and other metal isotopes may
exceed levels safe for human consumption.
It is concluded from this review that much remains to be learned about
the bioaccumulation of metals in aquatic organisms. Major areas of insuffi-
cient knowledge include the interconversions and pathways of metals in
natural environments, the relative contributions to the total tissue residue
of metals ingested from food compared to metals absorbed via respiratory
surfaces, the most bioaccumulative and toxic chemical species, and the
relationship between metal toxicity and metal residues in tissues. More
research is needed in these areas.
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CONTENTS
Page
Foreword iii
Abstract iv
Acknowledgments vi
I. Introduction 1
II. Conclusions and Recommendations 4
III. Aluminum 7
IV. Arsenic 8
V. Beryllium 11
VI. Boron 12
VII. Cadmium 13
VIII. Cesium 20
IX. Chromium 22
X. Cobalt 24
XI. Copper , 26
XII. Iron 29
XIII. Lead 30
XIV. Manganese 34
XV. Mercury 36
XVI.' Molybdenum 48
XVII. Nickel 49
XVIII. Plutonium 50
XIX. Ruthenium 52
XX. Selenium 54
XXI. Silver '. 56
XXII. Strontium 58
XXIII. Zinc 60
XXIV. General 68
References 74
Appendix. Index to scientific and common names of organisms 101
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ACKNOWLEDGMENTS
We are grateful to Robert V. fhurston for his guidance with this
project and for reviewing the manuscript and providing valuable comments.
We also thank Andrea Lawrence and Linda Eidet for their extensive work on
the References section and in helping to prepare the manuscript.
This research was funded by the U.S. Environmental Protection Agency,
Environmental Research Laboratory - Duluth, Research Grant No. R803950,
awarded to Natural Resource Ecology Laboratory, Colorado State University,
and Fisheries Bioassay Laboratory, Montana State University.
VI
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SECTION I
INTRODUCTION
During recent years considerable attention has focused on the fates
of metals and their derivatives in the aquatic environment. Although some
metals are essential to aquatic organisms in trace amounts, others offer no
known direct benefits. Mercury is an example of a non-beneficial metal which
is readily accumulated by aquatic organisms. The consumption of mercury-
contaminated fishes and shellfishes has resulted in several incidences of
human poisonings which have elicited worldwide concern over the dangers of
mercury in the aquatic environment. These incidences, as well as concern
for other aspects of environmental health, have prompted researchers to
explore the extent to which other metals are concentrated in living tissues,
particularly in aquatic organisms. In addition, the widespread development
of nuclear energy sources and the continued testing of nuclear weapons has
created concern over several metals isotopes.
Metals accumulation studies which focus on the aquatic environment
are important for various reasons. The extent to which metals are accumu-
lated by aquatic animals can be related to metals toxicity. The relationship
between acute toxicity and the concentration of metals in various tissues is
a useful tool for diagnosing the cause of fish kills, and knowledge of
relationships between chronic toxicity and metals tissue levels can aid
regulatory agencies in adopting and monitoring compliance with water quality
standards. Like mercury, other metals concentrated by commercially or
recreationally valuable aquatic organisms pose a threat to human consumers
and could thereby render these resources less valuable. The United States
Food and Drug Administration (FDA) currently lists mercury, lead, cadmium,
arsenic, selenium and zinc at the top of its priority list in its program
concerning toxic elements in food (Jelinek and Corneliussen 1977). Of
these, only mercury has an FDA-specified regulatory limit for fish and
shellfish (Anon. 1974); FDA guidelines for other metals in foods have not
been established. Survey and monitoring programs aimed at pinpointing
metals contamination problems would help regulatory agencies in adopting
the necessary restrictions, and an understanding of the processes governing
the fates, pathways and distributions of metals in natural waters is
necessary for assessing the current status of metals in the environment
and for avoiding potential problems due to metals.
Aquatic animals can assimilate metals by ingestion of particulate
material suspended in water, ingestion of food, ion exchange, and adsorption
on tissue and membrane surfaces. Excretion of metals occurs through the
feces, urine and respiratory membranes. In addition, animals with
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exoskeletons may lose considerable amounts of accumulated metals during
molting. A variety of physical, chemical, biological and seasonal variables
existing in natural waters interact to influence the availability of metals
to aquatic life. Moreover, certain metals or specific chemical species of
a given metal are accumulated and retained by fishes to a much greater degree
than others. Thus, the complexity of the factors governing metals uptake and
excretion precludes making widely applicable generalizations.
The purpose of this report is to collate the metals bioaccumulation
literature, particularly those studies dealing with metals bioaccumulation
by aquatic animals. Because the mercury literature has already been
thoroughly reviewed elsewhere, primary emphasis in the mercury section is
on recent publications. However, a few of the more important earlier find-
ings are summarized. A primary objective of this report is to evaluate
the importance of metals other than mercury from the standpoint of their
bioaccumulative tendencies; it should be recognized that other metals have
received only a fraction of the attention that mercury has. Twenty-one
metals covered individually in this review are aluminum, arsenic, beryllium,
boron, cadmium, cesium, chromium, cobalt, copper, iron, lead, manganese,
mercury, molybdenum, nickel, plutonium, ruthenium, selenium, silver,
strontium and zinc. A few additional metals which have received only
modest attention in the aquatic environment are covered in a general
section, Based on current understanding, recommendations are presented
as to which metals represent the greatest hazard to human consumers of
aquatic life and which are the least troublesome. Accounts published
after 1 July 1977 are not included in this report. Although this report
is extensive, it is not exhaustive; the authors accept full responsibility
for inadvertent omissions.
A few continually recurring terms should be defined at this point and
qualifying statements should be made. "Concentration factor" as used
herein refers to the ratio of the concentration (weight/weight) of a sub-
stance (in this case a metal) in an organism (or in a particular tissue
or organ) to the concentration (weight/volume) of that substance in the
water in which the organism had been living. For example, an organism
(or tissue or organ) containing 10 pg Cu g-1 taken from a lake containing
1 yg Cu a'1 has concentrated copper 10,000-fold; thus, by definition, the
concentration factor is 10,000. Concentration factors may be derived from
either laboratory or natural exposures to substances. "Concentration factors"
are most useful when they apply to organisms which had reached or had nearly
reached a plateau concentration of a substance under a particular exposure
condition. However, concentration factors are often derived and reported
for a pre-equilibrium stage in the accumulation of a substance, for purposes
of comparing various treatments in a laboratory experiment or for comparing
substance uptake rates among various organs or tissues from organisms in
a particular treatment. Thus, the exact conditions under which these con-
centration factors were derived should be known before comparing conceptra-
tion factors reported by different workers.
"Half-time" (or "half-life"), as used here, is biological half-time
and is defined as the amount of time required for an organism to eliminate
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half of the total body burden of an accumulated substance. Half-time is
a useful index of the relative persistence of metal residues in organisms.
Most workers express concentrations of substances in biological tissues
as the mass of substance present per mass of wet tissue; however, some
workers report concentrations on a dry weight basis. All metals concentra-
tions for biological substances reported in this review are wet tissue con-
centrations unless specified otherwise. In general, dry tissue concentrations
are enriched about fivefold over wet tissue values because most organisms
contain approximately 80 percent water.
The common and scientific nomenclature reported in the text is the
same as that used by the original author(s). Both common and scientific
names are included in most instances; however, a few of the most common
freshwater and marine fishes are referred to by their scientific name the
first time they are mentioned in a given section and by their common name
for subsequent referrals in the same section. In addition, some of the
less commonly known invertebrates are referred to only by scientific name.
The Appendix indexes text referrals to the various organisms.
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SECTION II
CONCLUSIONS AND RECOMMENDATIONS
Several trends are apparent from the information reported in this
review, and research and monitoring priorities are suggested.
1. Unlike mercury, most metals are not accumulated in the edible
portions of fishes and do not represent a threat to human consumers of fish
unless the fish are eaten in their entirety (Table 1). Metals deserving
further attention with respect to their propensity for accumulation in
edible fish tissues include mercury, arsenic and radioactive cesium.
2. Shellfishes, particularly oysters, passively accumulate many'
metals much more readily than fishes (Table 1); this suggests a priority
for monitoring in metal-contaminated area;s. Potentially dangerous metals
in shellfishes include cadmium, afsenfc, mercury',
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TABLE 1. THE RELATIVE HAZARD TO HUMANS PRESENTED BY THE OCCURRENCE OF
METALS IN THE EDIBLE PORTIONS OF FISH AND SHELLFISH
Bioaccumulative tendency
Metal
Aluminum
Arsenic
Beryllium
Boron
Cadmi urn
Cesium3
Chromium
Cobalt3
Copper
Iron
Lead
Manganese
Molybdenum
Mercury
Nickel
Plutonium3
Ruthenium3
Sel eni urn
Silver
Strontium
Zinc
to humans Freshwater
from oral fish
ingestion muscle
low high low high
X X
X X
X X
X X
X X
X X
X X
X X
X X
X X
X X
X X
X X
X X
X X
X C
X X
X X
X X
X X
X X
Marine Marine
fish shellfish or
muscle crustaceans
low high low high
x c
X X
c c
X X
X X
X X
X X
X X
X X
X X
X X
X X
x . c
X X
X X
X X
X X
X X
X X
X X
X X
Human hazard
rating
low med. high
x
x
x
x
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Radioisotope is primary form of concern.
Methylmercury is the species of concern.
Insufficient information available.
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6. Although some instances have been reported where high levels of
metals in natural waters have been attributed to natural sources, the
largest share of contamination is due to man. Waters receiving metals
inputs resulting from man's activities should receive the highest monitoring
priority.
7. The relationships between chronic toxicity thresholds and metal
concentrations in tissues have been determined for a few metals with a
few fish species. Studies should be undertaken to determine if these
relationships are valid in natural environments; if this concept proves
useful, then relationships should be established for other metals and
with other aquatic species.
8. Some chemical forms of metals, such as methylmercury, are far
more toxic and more readily accumulated by aquatic organisms than are
others. The most bioaccumulative and toxic forms of other hazardous metals
should also be determined.
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SECTION III
ALUMINUM
Aluminum is the commonest metallic element in the earth's crust; it is
abundant in many rocks and ores but does not occur as pure aluminum in
nature. It accumulates in the lungs of humans but is almost nontoxic
to man (Berry ejt aJL 1974). Aluminum is an essential metal for human
biological function, although its function in tissues has not been clearly
established; aluminum levels 5 to 50 times the normal daily intake do not
appear to be harmful to humans (Sorenson et al. 1974). Aluminum may enter
natural waters from coal strip mining activities (Sorenson et_ al_. 1974),
as a byproduct of some oil shale mining processes (Freeman and Everhart
1971), from water treatment facilities using aluminum sulfate (alum) as
a coagulant for suspended solids (NAS 1973), and in industrial wastes.
Aluminum is amphoteric in water, the solubility of- aluminum hydroxide
complexes increasing both above and below pH 5.5 (Burrows 1977). However,
the conditions existing in most natural waters cause aluminum to be pre-
cipitated or absorbed (Kopp and Kroner 1970).
To our knowledge, no laboratory experiments have been completed on
the uptake and elimination of aluminum by aquatic organisms; however,
several workers have reported aluminum residue concentrations in marine
and freshwater fishes. Eviscerated, decapitated lake trout (Salvelinus
namayaush) from a New York lake averaged from 140 to 300 yg Al g"1 depending
on their age; however, aluminum content was not age-related. Calico bass
(Paraldbrax clathratus) collected near Catalina Island, California, averaged
8.0 and 25 yg Al g"1 of dry tissue in muscle and liver respectively (Stapleton
1968). Comparatively, calico bass collected near the outfall of a Los
Angeles steam plant contained 25 yg Al g-1 in muscle and 28 in liver on a
dry basis. Dover sole (Miorostomus pacificus) collected near municipal
outfalls along the southern California coast contained, on a dry basis, 1.8
to 8.2 yg Al g-1 in kidney and 0.6 to 15 in heart (McDermott et al_. 1976).
Goldberg (1962) determined the elemental composition of ashed tissue samples
from yellowfin tuna (Neothunnus macropterus). The highest percentages of
aluminum compared to other salts were found in heart, pyloric caeca, liver
and spleen; however, the concentrations of aluminum in these tissues were
not reported.
Consumption by humans of seafoods containing aluminum presents little
risk due to the low toxicity of aluminum to humans. Moreover, the insolu-
bility of aluminum under many natural conditions decreases aluminum's
importance as a toxicant in water. However, both the toxicity of aluminum
to aquatic life under those conditions promoting aluminum's solubility and
the aluminum tissue levels resulting in adverse effects on aquatic organisms
are poorly understood and warrant further investigation.
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SECTION IV
ARSENIC
Arsenic is widely used as an herbicide to defoliate cotton before
mechanical picking. Furthermore, the smelting of ores and the burning of
fossil fuels contribute significant amounts of arsenic to the atmosphere.
Arsenic is known to have a high affinity for sulfhydryl groups in proteins
and thus interferes with certain enzymatic reactions (Berry e_t al_. 1974).
Acute poisonings in humans are characterized by gastrointestinal problems,
irregular heartbeat, coma and possibly death. Chronic exposure symptoms
include alimentary canal disturbances, coughing, and graying of the skin.
Respiratory and skin diseases have been reported among smelter workers and
members of an adjoining community (Birmingham ejt al_. 1965). Some reports
suggest that arsenic in drinking water may increase the incidence of skin
cancer (NAS 1973). Arsenic may. reach the aquatic environment through
atmospheric fallout, industrial outfalls and the improper application of
arsenical herbicides or pesticides (Sandhu 1977). In water, trivalent
arsenic (arsenite) is far more poisonous than the pentavalent form (arsenate);
however, under aerobic conditions trivalent arsenic is quickly converted to
arsenate (Dabrowski 1976). In addition, arsenic may be bacterially
methylated, much like mercury, to form highly toxic methylarsenic or
dimethylarsenic (Anon. 1971; Braman and Foreback 1973). Fortunately,
these compounds are volatile and are readily oxidized to less toxic forms
(Wood 1974).
Gilderhus (1966) observed arsenic uptake by young and adult bluegill
(Lepomis macrochirus] placed in ponds treated with various concentrations
of the herbicide sodium arsenite. By the end of the test arsenic concen-
trations in water ranged from 0.3 to 9.0 mg As jr1. After sixteen weeks'
exposure whole adult bluegills contained arsenic levels very similar to
the concentration of arsenic remaining in the pond after that period.
Muscle arsenic concentrations in mature fish were about 60' percent that
of whole fish. Immature bluegills attained arsenic concentrations nearly
twice those present in adults. Immature bluegills displayed reduced sur-
vival and growth rates in proportion to the level of arsenic in the pond;
adult survival, however, was decreased only at the highest arsenic concen-
tration. Tissue residues of 1.3 and 5.0 yg As g"1 were associated with
reduced growth rate and increased mortality in immature and adult bluegills
respectively. By the end of the experiment, 20 to 80 percent of the arsenic
applied to the ponds remained in solution.
Dabrowski (1976) incubated rainbow trout (Salmo gairdneri) eggs in
water containing various concentrations of either sodium arsenate or arsenic
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trioxide. The same pattern of arsenic accumulation was observed for both
compounds. Embryos accumulated up to 2.5 yg As g"1 after 40 days' exposure
to only 0.05 mg 2"1 arsenic. Accumulation of arsenic became accelerated
between 33 and 41 days of exposure, presumably due to increased permeability
of the chorion during this stage of development. Concentrations up to 50.0
mg As jr1 did not reduce egg survival; in fact, reduced survival was observed
at arsenic concentrations less than 5.0 mg jr1 because the higher arsenic
concentrations reduced fungal growth on eggs.
Sorensen (1976a) exposed green sunfish (Lepomis cyanellus] to various
concentrations of arsenic (as sodium arsenate) in water and measured accumu-
lation of the metal. There appeared to be a relationship between exposure
concentration and arsenic accumulated, but the data were quite scattered.
In another study (Sorensen 1976b) green sunfish were exposed to the same
chemical under varying temperatures and exposure intervals. Arsenic uptake
by liver, gut and muscle increased with arsenic concentration in water,
temperature and exposure interval. Dead sunfish did not passively accumulate
arsenic, and no useful method was found for confirming arsenic-caused fish
kills. Biological half-time for arsenic in gut and liver was about seven
days. Because arsenic has been used to control aquatic vegetation, Wiebe
et al. (1931) examined the background levels of arsenic in largemouth bass
~(Mier>opterus salmoides) from several Illinois rivers and then measured
accumulation of arsenic by the bass after exposure to arsenic in food and
water. Although arsenic was readily accumulated from both sources, elimina-
tion was rapid upon termination of exposure. The arsenic levels necessary
to control aquatic vegetation did not result in arsenic concentrations in
bass considered to be dangerous to human consumers of fish. Similarly,
Ullmann et_ aj_. (1961) compared the arsenic content of calico bass (Pomoxis
nigromaaula-tus} collected from New York lakes before and after treatment
with the herbicide sodium arsenite; no differences were detected. Fish
contained between 0.10 and 0.47 yg As g"1 in muscle fillet.
Pakkala ejt al_. (1972) surveyed arsenic concentrations in decapitated
eviscerated fishes from various New York lakes. The maximum level reported
was about 0.5 yg g"1, and for a given location fish age did not appear to
be correlated with tissue residues. Sandhu (1977) measured arsenic content
of fish and water in a pond accidentally sprayed with an arsenical herbicide.
Arsenic in the pond reached 2.5 mg As JT1; fish accumulated up to 12.4 yg As
g-1 in muscle representing a concentration factor of only five. Ellis et a_1.
(1941) surveyed the arsenic content of various freshwater fish species
collected from southeastern United States waters; the average arsenic
content for all species was 0.75 yg As g*1. Lipids contained more arsenic
than other fractions; in particular, liver oil averaged nearly 40.5 mg As
JT1. Lake Michigan plankton and benthos were found to contain 6.0 and 6.6
yg'As g-1 respectively (Seydel 1972); Lake Superior plankton contained
about 30 percent less. The arsenic concentrations present in phytoplankton
and zooplankton were similar.
The arsenic levels in some marine organisms have also been measured.
LeBlanc and Jackson (1973) analyzed various marine organisms from the
western coast of Canada and found that muscle tissue from assorted fishes
and clams usually contained between 1 and 5 yg As g"1, but dungeness crab
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(Cancer magister] muscle averaged nearly 7 yg As g"1 with one individual
containing 37.8 yg As g"1. Wilber (1969) has reported arsenic levels in
marine shellfish exceeding 100 yg g-1. These values are considerably
higher than those reported for freshwater organisms. Uthe and Reinke
(1975) have demonstrated that post-mortem tissues from fish, shellfish
and lobsters were capable of reducing arsenate to the highly toxic arsenite.
Evidence suggests that the reduction is chemical. This accounts for the
finding that arsenic found in tissues from these organisms collected in
nature exists almost entirely as arsenite.
Arsenic is accumulated by fishes both from water and from food but
reported concentration factors for arsenic in fishes are generally quite
low. Arsenic is lipophilic; thus, fats contain more arsenic than other
tissue fractions. Fish muscle tissue also accumulates arsenic; however,
the biological half-time of arsenic is only seven days in green sunfish.
Shellfishes concentrate arsenic to a much greater degree than fishes, and
marine organisms contain more arsenic than freshwater forms. The U.S. Food
and Drug Administration (FDA) allows 3,5 yg As g"1 in fruits and vegetables,
and Canadians recommend a maximum level of 5.0 yg As g-1 for food (NAS
1973). These guideline levels have reportedly been exceeded 20-fold in
shellfish and more than twofold in fish, but surveys of arsenic in fishes
have shown that they usually contain substantially less arsenic than the
guideline recommends. Shellfishes, therefore, warrant special attention
because of their unusual metals-concentrating ability. Like mercury,
arsenic can apparently be methylated by microorganisms in water, but the
frequency of this occurrence and the bioaccumulative properties of methylated
arsenicals have not been reported. More research is needed regarding
methylated arsenicals. Arsenate present in the tissues of consumable sea-
food organisms is rapidly converted to arsenite following death; thus,
arsenic in marketable seafoods is likely present in one of the most poison-
ous forms.
10
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SECTION V
BERYLLIUM
Beryllium was at one time used to coat fluorescent lights and is
currently used as a hardening agent in metal alloys, an additive in
rocket fuels (McKee and Wolf 1963), a catalyst in the electroplating and
organic chemical industries (NAS 1973), and a structural material for
missiles and spacecraft; it is also used in nuclear reactors as a reflector
or moderator and in gyroscopes and computer parts (Weast 1975). Signifi-
cant amounts of beryllium also occur in the ores of other metals and in
coal. Beryllium poisonings in humans (beryl!iosis) have resulted from
industrial exposures to beryllium dusts or fumes in or near beryllium
refineries; however, reports indicate that orally ingested beryllium is
not toxic to humans (Berry et_ al_. 1974). Symptoms of poisoning include
pneumonitus and coughing, fatigue, and weakening of the heart (Knapp 1971).
Beryllium metal is insoluble in water, as are its carbonate, oxide and
sulfate; however, beryllium nitrate, phosphate and halides are all water-
soluble (Weast 1975). Little work has been completed concerning the fates
and pathways of beryllium in water. Tarzwell and Henderson (1960) have
demonstrated that beryllium is highly toxic to warmwater fishes in soft
water.
Slonim (1973) measured 7Be uptake by guppies (PoeciUa reticulata) in
a static freshwater system. Levels were highest in the viscera and intes-
tinal tract followed by kidney and ovary. Uptake was directly related to
beryllium concentration in water, inversely related to fish size, and not
related to fish age. Water hardness was inversely related to beryllium
toxicity but did not influence beryllium uptake by the guppies. Thus,
body burden of beryllium is not the controlling factor governing toxicity.
The authors suggested that beryllium present in a particular target organ
may be related to toxic response.
Although beryllium has a low solubility in water, it is possible that
benthos could accumulate beryllium from sediment and thereby transfer the
metal to higher organisms via the food chain; however, the danger of
beryllium in consumable products to man is minimal because orally ingested
beryllium has a low toxicity. Although beryllium toxicity decreases with
increasing water hardness, beryllium uptake is unaffected by increasing
hardness. Due to the paucity of information concerning the accumulation
of beryllium by aquatic animals and because of beryllium's high toxicity
under certain conditions, more work is needed concerning the relationship
between beryllium accumulation by aquatic animals and beryllium toxicity.
11
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SECTION VI
BORON
Boron is used in a process for bleaching groundwood by the pulp and
paper industry (Thompson ejt aj_. 1976), as a hardener for other metals, and
as a neutron absorber in nuclear installations (NAS 1973); it is also
enriched to a considerable degree in fly ash from fossil fuels. Boron
exists naturally at high concentrations in seawater as borate (NAS 1973).
Boron has a relatively low toxicity to mammals as evidenced by the observa-
tions that cattle have consumed nearly 20 g of borax per day and humans
3 g boric acid per day with no adverse symptoms (McKee and Wolf 1963), but
only 1 mg B a~l in irrigation water is toxic to some plants (Kopp and
Kroner 1970).
Igelsrud ejt al. (1938) measured boron levels .in marine algae and found
that terrestrial pTants growing" in solutions'containing boron levels similar
to those existing normally in seawater accumulated higher boron concentra-
tions than the marine algae. Calcareous structures such as the shells of
marine organisms concentrated boron to a considerable degree. The authors
suggested that boron in these structures was likely present as magnesium or
calcium borate. The boron contents of various freshwater and neritic and
oceanic marine zooplankton and phytoplankton have also been measured
(Yamamoto e_t al_. 1973). Generally, zooplankton contained higher boron
levels than phytoplankton in the marine environment but phytoplanktons
were higher in freshwater. Marine neritic forms contained more boron on
the average than oceanic forms. Interestingly, little difference existed
in the boron content of the freshwater forms compared to marine species
even though the boron content of seawater averages about 460 times that
of freshwater.
Thompson e_t al_. (1976) measured boron accumulation and elimination in
underyearling sockeye salmon (Oncorhynehus nerka] and in juvenile oysters
(Crassostrea gigas] and found that boron was only modestly accumulated and
readily eliminated. In sockeye salmon, bone contained the highest boron
concentration followed by gill, liver and kidney. They also surveyed
various shellfishes from British Columbia waters and found that the boron
content ranged from about 1 to 6 yg g"1.
In view of the fact that boron is a normal constituent of salinity in
seawater, has a relatively low toxicity to aquatic animals and to man and
is not readily bioconcentrated by aquatic organisms, boron is probably not
a serious pollutant in the aquatic environment.
12
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SECTION VII
CADMIUM
Cadmium is rare in nature, but is highly toxic. Cadmium poisonings in
humans resulting from oral consumption or inhalation of the metal are well
documented (Flick e_t a]_. 1971; Fassett 1975) with most exposures occurring
in industry. Chronic exposures to cadmium are believed to contribute to
cardiovascular diseases, hypertension and cancer. Voors and Shuman (1977)
were able to correlate liver cadmium levels with the incidence of heart
failure in North Carolina residents. One of the more tragic incidences of
cadmium poisoning occurred among rice paddy workers in Japan; exposure re-
sulted from the practice of using mine water to irrigate rice fields (Martin
1971). Workers developed a skeletal disorder resulting in bones so fragile
that just coughing caused multiple fractures of limbs and ribs. Major
sources of cadmium in natural waters include effluents from electroplating
and smelting industries and runoff from agricultural areas where phosphate
fertilizers are used (Clubb ejt a]_. 1975).
Several authors have measured cadmium uptake by freshwater organisms
following short exposures to high levels of cadmium in water. Solbe and
Flook (1975) examined cadmium concentrations in vertebrae and muscle from
stone loach (Noemacheilus barbatulus) exposed to cadmium concentrations
bracketing acutely lethal levels and found a direct relationship between
concentrations of cadmium in water and in tissue. Clubb ejt al_. (1975)
measured cadmium uptake and elimination in two stoneflies, Pteronarcella
badia and Pteronavcys calif'arnica, exposed to subacute levels of cadmium
followed by return to cadmium-free water. Uptake was curvilinear in both
species while elimination was rapid and linear. The latter result suggests
that these insects may be capable of recovering from intermittently high
exposures to cadmium.
The distribution of cadmium among various tissues and organs from
freshwater fishes has also been examined. Rowe and Massaro (1974) looked
at the change in body distribution of cadmium over 21 days in white catfish
(Ictalurus oatus] following administration of a single intragastric dose
(0.2 mg Cd kg"1). Concentration maximums for gastrointestinal tract organs
were reached shortly after injection. Organs continuing to increase in
cadmium concentration after 21 days included liver, kidney, spleen, swim-
bladder, blood and ovaries with kidney and liver containing the highest
concentrations. The authors postulated that perhaps metallothionein was
being synthesized by liver and kidney thereby facilitating the detoxifica-
tion process. Marafante (1976) has confirmed that all the cadmium present
in the livers and kidneys of goldfish (Carassius auratus] was associated
13
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with a specific cadmium-binding protein and Noel-Lambot (1976) has demon-
strated the existence of a cadmium-binding protein in the mussel ifytilus
edulis.
Mount and Stephen (1967) were able to correlate cadmium mortalities
in bluegill (Lepomis maoroahirus] to the amount of cadmium accumulated in
gill tissue. Fish killed by cadmium always contained more than 150 ug Cd
g-1 in gill whereas survivors never exceeded 130 yg Cd g"1. The authors
speculated that gill autopsy may be useful for confirming cadmium-caused
fish kills. It was further shown that liver accumulated high concentrations
of cadmium during chronic exposure but accumulated very little following
acute exposure; it was suggested that fish liver concentrations exceeding
300 yg Cd g*1 indicate a previous history of chronically damaging cadmium
exposure.
Others have studied cadmium uptake in freshwater fishes exposed to
sublethal concentrations of cadmium over an extended time period. Rehwoldt
(1976) fed adult zebrafish (Braehydanio rerio) a diet containing 10 yg g"1
cadmium for six months and measured cadmium uptake in whole fish. Male
zebrafish accumulated over twice as much cadmium as females. Uptake pro-
ceeded linearly for two to three months then leveled off, becoming asymp-
totic over the last three to four months of exposure. This dietary cadmium
level resulted in a marked decrease in reproductive success; however, very
little cadmium was present in newly hatched young. Pascoe and Mattey (1977)
exposed three-spined stickleback (Gasterosteus aculeatus) to various cadmium
concentrations in water (0.001-100 mg Cd £"1, hardness near 100 mg £-1 as
CaCOs) for up to 79 days. Stickleback accumulated cadmium at all concen-
trations tested; however, concentration factor was inversely and linearly
related to exposure concentration. Concentration factors ranged from 511
at the lowest exposure to 0.51 at the highest. All of the concentrations
tested were lethal to stickleback.
Kinkade and Erdman (1975) measured 115Cd uptake by various organisms
in both hard (150 mg a-1 as CaC03) and soft (0 mg £-1 as CaC03) water.
After 21 days' exposure the infusoria snail (Ampullaria paludosa], catfish
(Corydoras punctatus) and guppy (Lebistes retiaulatus) held in soft water
had all accumulated higher cadmium concentrations than individuals held in
hard water. Hardness influenced cadmium uptake by the guppies more than
the other species; by the end of the experiment, guppies kept in soft water
had accumulated over twice as much 115Cd as the hard water group. On the
other hand, cadmium uptake by catfish was only slightly reduced by hardness.
Interestingly, both snail and catfish accumulated cadmium more rapidly in
hard water during the first few days of exposure to the isotope but the soft
water groups eventually caught up and surpassed those held in hard water;
guppies accumulated cadmium more readily in soft water from the onset.
Guppies accumulated cadmium much more readily than catfish, reaching levels
almost 12-fold that of catfish by the end of the experiment. These results
may partly explain the increased toxicity of cadmium to fish in soft water
and the relative resistivity of catfish to cadmium toxicity.
Benoit ejt al_. (1976) measured cadmium levels at various time intervals
in several tissues from brook trout (Salvelinus fontinalis) exposed to
14
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cadmium in water for up to 38 weeks. Kidney accumulated the highest concen-
trations of cadmium followed by liver and gill. Muscle did not accumulate
significant amounts of cadmium at any of the concentrations tested, including
levels at or above the lowest concentration found to be chronically damaging
(3.4 yg Cd ir1). Most tissues appeared to reach equilibrium with respect
to cadmium after 20 weeks. The authors suggested that equilibrium cadmium
levels could prove to be a useful index for determining the fitness of
cadmium-exposed fish populations in nature. Fish placed in fresh water
after previous exposure to cadmium lost cadmium rapidly from gill tissue
but did not lose cadmium from either kidney or liver. Similarly, Kumada
et al. (1973) measured the uptake and retention of cadmium by rainbow trout
^Salmo gairdneri] exposed to cadmium in water for up to 40 weeks; the fish
attained maximum cadmium concentrations after 10-20 weeks' exposure with
liver and kidney having the highest concentrations. Return to freshwater
resulted in rapid loss of cadmium by gills, extended elimination by most
organs, and almost no loss of cadmium from kidney. These cadmium clearance
patterns suggest that gill is the major site of cadmium accumulation from
water and kidney is the route of elimination. —
Cearley and Coleman (1974) exposed largemouth bass (Micropterus
salmoides) and bluegill to various concentrations of cadmium for periods
of up to six months and measured cadmium concentrations in gill, gut content
and remaining tissue after various time intervals. Gut content contained
the highest cadmium levels followed by gill and remaining fish. All tissues
reached equilibrium after two months, a shorter time period than that found
by Benoit e_t al_. (1976); however, the water temperatures were considerably
higher (23.9 C compared to 3-15 C) during this experiment. Behavior of
dying fish suggested that the nervous system was affected. Piavaux (1977)
tried to determine the influence of cadmium on zinc metabolism by exposing
sunfish (Lepomis gibbosus] to cadmium in water and measuring changes in
activity of the Zn-metalloenzyme alkaline-phosphatase in various organs in
addition to measuring changes in zinc and cadmium concentrations in these
organs. Exposure to cadmium resulted in cadmium accumulation by all organs
analyzed whereas zinc increased in some organs and decreased in others.
The activity of the enzyme did not follow any systematic trend. The authors
thus concluded that cadmium does not preferentially out-compete zinc for
the active metabolic sites involved in this system.
In another chronic study Eaton (1974) exposed bluegill to cadmium in
hard water at levels ranging from 31 to 2140 yg Cd jr1. After 11 months'
exposure tissue residues were measured in gill, intestine and caecum,
liver, and kidney. Although individuals held at all cadmium concentrations
contained considerably more cadmium than controls, differences between fish
held in the various treatments were not that great. The no-effect level
was between 31 and 80 yg Cd jr1.
Cadmium uptake by marine organisms has also been extensively studied.
Calabrese ejt aJL (1975) measured the concentrations of cadmium in gill and
blood from winter flounder (Pseudopleuronectes americanus) exposed to 5 or
10 yg Cd JT1 in water but no cadmium was detected. Dethlefsen et al. (1975)
subjected eggs and larvae of herring (Clupea harengus), garpike~TBek?ne
belone), and flounder (Platichthys flesus] to several cadmium concentrations
15
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in water at various salinities for up to 14 days. Garpike accumulated
considerably less cadmium for a given cadmium concentration in water than
did flounder or herring. It was postulated that the garpike chorion was
more efficient at retaining cadmium, thus newly hatched larvae would begin
with less cadmium. Only fish exposed to 0.5 mg jr1 cadmium and higher
accumulated more cadmium than controls, and salinity did not influence ac-
cumulation. Although earlier studies had shown.that embryos accumulate
cadmium, larvae were shown to accumulate cadmium much more rapidly than
embryos.
Maclnnes et_ a]_. (1977) exposed cunner (Tautogoldbrus adspersus] to
either 0.05 or 0.10 mg Cd a,'1 in seawater for 30 or 60 days. All tissues
analyzed (gill, muscle, liver) contained cadmium concentrations below the
detection limits (2.0 yg Cd g'1) for the methods used. However, Benoit et_
al. (1976), using a much more sensitive analytical method, detected sig-
nificant uptake for the same tissues at concentrations even lower than
those to which fish were reportedly exposed in the above study. Therefore,
the analytical methodology employed probably obscured the results.
In another study Greig ejt ajk (1974) measured cadmium uptake and
elimination in cunner exposed to concentrations of cadmium in seawater
ranging from 3 to 48 mg jr1. Liver attained the highest cadmium level,
averaging 8.2 times higher than gill.' The relationship between cadmium
concentration in water and that in liver was linear, but the relationship
appeared curvilinear for gill. Upon transfer to clean water, cunner
rapidly cleared cadmium from gills, red blood cells, and serum and retained
cadmium in muscle and carcass. Cadmium elimination from liver was highly
variable with some fish clearing cadmium rapidly and others retaining high
levels of cadmium in liver.
Several cadmium uptake experiments have been performed with mummichog
(Fundulus heteroalitus] (Eisler 1971, 1974). Pertinent findings included:
(1) Survivors accumulated a proportionally smaller percent of the cadmium
in their medium with increasing concentration whereas fish that died ex-
hibited the reverse trend. (2) Tissue concentrations exceeding 86 mg Cd
kg-1 ash were usually lethal. (3) After 21 days of exposure, viscera con-
tained more than 60 percent of the total cadmium, gill had 22 percent, and
head and remainder had 8-10 percent. (4) Fish placed in cadmium-free water
for 180 days after a 21-day cadmium exposure period lost about 90 percent
of their accumulated cadmium; viscera contained most of the retained cad-
mium. (5) Fish exposed to various cadmium concentrations'in water for
periods ranging from 6 to 96 hours and then placed in cadmium-free water
for 50 days accumulated cadmium levels proportional to their exposure
regime and eliminated 54-76 percent of the accumulated cadmium during the
post-exposure period. (6) Dead mummichog accumulated cadmium much more
rapidly than living individuals; e.g., 89 times as much after 48 hours'
exposure and 53 times as much after 24 hours' exposure. (7) Elimination
rate of cadmium was somewhat greater for dead fish but at most only four
times greater than survivors. The same author and coworkers (Eisler e_t al_. ,
1972) have shown that American oysters (Crassostrea virginica] were able to
concentrate cadmium in edible tissues from seawater to a much greater
degree than either mummichog, bay scallop (Aquipecten irradians) or American
16
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lobsters (Homarus americanus). Cadmium concentrations exceeding levels con-
sidered dangerous for human consumption (13 mg kg'1) were attained by oysters
exposed to cadmium concentrations in water considered safe for drinking
(10 yg A'1)- Zaroogian and Cheer (1976) reported that American eastern
oysters (c. virginica) reached the 13 mg kg-1 level after exposure to only
5 yg Cd JT1 for 40 weeks. American oysters exposed to either 0.1 or 0.2
mg Cd Jr1 in seawater experienced heavy mortalities after 13-16 weeks
preceded by emaciation and discoloration (Shuster and Pringle 1969).
Oysters exposed to both cadmium levels accumulated about 100 yg Cd g"1 after
13 weeks. Comparatively, American oysters collected from the Atlantic coast
of the United States contained 0.08 to 7.78 yg Cd g'1 (Pringle et al_. 1968).
O'Hara (1973) found that cadmium accumulation in the estuarine fiddler
crab (lloa pugilator] was directly related to temperature and inversely
related to salinity. The salinity effect was believed to result from the
necessity for the crab actively to accumulate salts as salinity decreased.
Similarly, Wright (1977a) found that increasing salinity decreased cadmium
accumulation in the haemolymph and carapace of the shore crab (Carcinus
maenas); however, salinity didn't influence cadmium uptake by either gill
or hepatopancreas. In particular, calcium was found to be responsible for
this effect (Wright 1977b). In another study using the shore crab Wright
(1977c) found that haemolymphatic cadmium was almost totally bound to the
protein fraction. Cadmium levels in the haemolymph tended to rise immedi-
ately preceding mortality. Cadmium uptake was believed to be passive, but
active uptake was not eliminated as a possibility. Cadmium uptake by marine
bivalves (Mya arenaria, Mytilus edulis, Mulinia lateralis and Nucula proxima]
increased with increased temperature and decreased with increasing salinity;
however, the magnitude of the response varied with species (Jackim et al.
1977). Moreover, the presence of sediment or zinc ions acted to decrease
cadmium accumulation. The sediment effect was attributed in part to a
reduced filtration rate observed in bivalves living in sediment. Among
these four species, filter feeders accumulated more cadmium than deposit
feeders.
Fowler and Benayoun (1974) described the uptake, elimination and reten-
tion of 109Cd in both the mussel Mytilus galloprovinciaUs and the benthic
shrimp Lysmata seticaudata. Test organisms were still accumulating cadmium
at the end of two months' exposure to cadmium in water. After this time
whole mussels had reached a concentration factor of 130 and whole shrimp 600.
Both organisms attained highest cadmium levels in viscera although exposure
was only through water. Interestingly, cadmium uptake and elimination rates
were directly related to temperature in shrimp but unaffected by temperature
in mussel. Biological half-times for test organisms held in the laboratory
were 378 days for shrimp and 1254 days for mussel; however, mussels kept
in cadmium-free water in the laboratory eliminated cadmium more slowly than
animals kept in an estuary. This was believed to result from the laboratory
animals being of a poorer nutritional state. Kerfoot and Jacobs (1976)
measured cadmium uptake at various levels of a marine food chain consisting
of sewage-seawater, plankton and shellfish. Components of the food chain
were cultured separately in a sewage treatment system designed to utilize
nutrients from the sewage to provide algae indirectly to be used as food
for the shellfish population. In this system cadmium accumulated by the
17
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algae was a more important source of cadmium to shellfish than was cadmium
in water. However, the authors believed that the importance of these two
sources would be reversed in a natural system.
Several surveys of the concentrations of cadmium in various marine
and freshwater biota have been completed. Havre e_t aJL (1973) measured
cadmium levels in several marine fish species caught off the coast of Norway.
Cadmium levels were very low for all fish tested, ranging from 0.002 to
0.033 pg Cd g"1. Lovett e_t aj_. (1972) examined cadmium concentrations in
eviscerated, decapitated fish from various freshwater lakes and streams in
New York state. Maximum concentrations exceeded 0.1 pg Cd g*1 but most
fish contained less than 0.02 pg Cd g"1. Talbot e_t a]_. (1976) measured
cadmium levels in oysters and mussels from Port Philip Bay and Corio Bay
near Melbourne, Australia. Both shellfish were highly contaminated, with
oysters containing more cadmium than mussels. Oysters contained from 35.5
to 174.3 pg Cd g~* and mussels ranged from 2.8 to 17.0 pg Cd g-1. Mussels
collected from piers contained less cadmium than mussels living on sediment,
implicating sediment as a contributor to uptake. Martin and Broenkow (1975)
found that mixed phytoplankton and zooplankton collected off Baja, California,
near San Diego averaged 13.2 pg Cd g'1 (dry weight basis); samples collected
from other coastal areas never exceeded 7.5 pg Cd g-1. Cadmium levels
averaged between 184 and 1163 pg Cd g"1 (dry basis) in red abalone (HalioHs
rufesoens} from various portions of the California coast (Anderlini 1974).
Preston (1973) discussed the sources of cadmium to marine waters off the
coast of the United Kingdom. Industrial effluents were the greatest con-
tributors to cadmium in the ocean with atmospheric fallout not considered
an important source. Major contamination problems were limited to inshore
waters. Shellfishes, particularly oysters and crabs, contained the highest
cadmium concentrations.
Cadmium is readily accumulated through both food and water by marine
and freshwater organisms, and either source of uptake can result in the
development of toxic symptoms by fishes. Fish tissues appear to reach
equilibrium with respect to cadmium after 8-20 weeks' exposure, depending
on the water temperature. Cadmium uptake increases with increasing water
temperature and decreasing salinity. Sex may determine rate of cadmium
accumulation in some fish species, perhaps due to sex-related metabolic
differences. Fish accumulate highest cadmium concentrations in kidney and
liver, probably due to the presence of a detoxifying cadmium-specific binding
protein. High concentrations of cadmium in fish liver may indicate a history
of chronic cadmium exposure.
An autopsy technique has been developed for freshwater fishes utilizing
the finding that a survival threshold concentration exists for gill tissue.
However, this technique is probably not useful in the marine environment
because dead fish placed in cadmium-spiked saltwater accumulated cadmium
at a far greater rate than living individuals. This phenomenon possibly
occurs because of the hypertonic nature of the saltwater medium. Chronic
cadmium poisoning appears to be correlated with specific tissue cadmium
levels, perhaps providing a method for detecting the occurrence of adverse
cadmium conditions in natural environments.
18
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Very little cadmium is accumulated in the edible portions of fishes.
Cadmium in fishes, therefore, does not appear to represent a hazard to
human consumers. However, oysters, abalone and mussels are capable of
accumulating extremely high levels of cadmium in edible portions and
therefore represent a greater hazard to human consumers than other marine
organisms. Because of cadmium's high toxicity, edible shellfishes should
be carefully monitored whenever cadmium contamination is suspected.
19
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SECTION VIII
CESIUM
Nuclear testing in the years following World War II has resulted in
the release of considerable amounts of cesium into the environment. In
addition, radiocesium is a component of discharges from nuclear power
plants and fuel reprocessing plants (Hewett and Jefferies 1976). Cesium
has a relatively low toxicity to humans; however, radiation sickness may
result from exposure to the radioisotope.
Brungs (1967) found that most of the 137Cs introduced into a pond was
associated with the sediment within four days following application; however,
tadpoles accumulated a considerable amount of the isotope. In another pond
study, Pendleton (1959) found that 137Cs concentration factors for different
organisms were directly related to- trophic .level-. Cesium-137 levels in
sunfish (Lepomis gibbosus) from th'e pond fluctuated widely during the 15-
month experiment; lowest concentration factors in sunfish occurred during
high and low temperature extremes.
Few studies have dealt with the distribution of cesium in fish, but
the Nile catfish (Clarias lazera) concentrated mCs to the greatest extent
in muscle and bone (Ishak e_t al_. 1977). The concentration factor (based on
dry weight) at maximum uptake was only 0.37. Gustafson et^ al_. (1966)
measured the 137Cs content in the edible portions from selected marine and
freshwater fish species purchased from Chicago area fish markets. Fresh-
water fish contained much higher 137Cs concentrations than marine species,
and carnivores generally contained higher concentrations than planktivores.
Cesium concentration factors for marine fishes were as low as 20 whereas
some freshwater fish concentrated cesium nearly 10,000-fold. An indirect
correlation was found between the level of potassium in water and the
ability of fish to accumulate radiocesium. Other workers have reported a
similar finding (Williams and Pickering 1961; Feldt 1963; Preston et al.
1967). Thus, less cesium is accumulated by fishes living in the potassium-
rich marine environment.
Morgan (1964) compared 13l*Cs uptake among various freshwater and
marine organisms and determined thejnfluence of organism size on uptake
and elimination of the isotope. The rate of cesium uptake among the
various organisms was compared by determining the amount of time required
for the organisms to attain a concentration factor of unity. Trends that
were noted included: (1) Marine shellfishes, including various crustaceans
and molluscs, and marine pelagic fishes reached a concentration factor of
unity in four days or less; (2) marine'demersal and bottom feeding species,
20
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freshwater mussels and marine eels required 6 to 17 days to attain unity
with respect to the isotope; (3) rays and freshwater fishes required between
30 and 120 days to attain unity; (4) freshwater organisms concentrated
13uCs tenfold greater than marine organisms; and (5) rate of uptake and
half-time of elimination were inversely related to organism size. Depending
on the organism, rates of uptake varied up to eightfold over the range of
sizes tested. Half-time of elimination decreased about 3.5-fold with a
100-fold increase in organism weight.
In a saltwater laboratory study Baptist and Price (1962) looked at
137Cs accumulation and elimination by summer flounder (ParaHchthys
dentatus], croaker (Miaropogon undulatus), bluefish (Pomatomus saltatrix)
and little tuna (Euthynnus alleteratus]. Cesium was readily accumulated
both from food and from water. Concentration factors for all species
ranged from 10 to 20. Cesium elimination rate functions varied among
tissues. The half-time for edible muscle tissue approached 100 days.
Hasanen and Miettinen (1963) noted that fishes collected from Finnish
lakes contained 137Cs in proportion to their po'sition in the aquatic food
chain, suggesting that food was an important route of uptake. Similarly,
Jefferies and Hewett (1971) described the importance of various sources
of cesium accumulation in plaice (Pleuronectes platessa L.) and thornback
ray (Raja clavata) and determined biological half-times. Ray were estimated
to derive over 80 percent of their cesium from food whereas plaice derived
approximately 50 percent via this route. A significant route of cesium
uptake from water for plaice was through the gut. The biological half-
time for cesium in ray was calculated to be 180-190 days and in plaice
120-140 days. Excretion of cesium was primarily extrarenal. In another
experiment Hewett and Jefferies (1976) exposed brown trout (Salmo trutta)
to 137Cs in freshwater and found a concentration factor near 10 for muscle
and a biological half-time of about 100 days. This low concentration
factor is similar to those reported for marine fish but probably is a
result of the high potassium content of the test water (4.0 mg 5,"1)-
Earlier work (Preston e_t al_. 1967) had shown that the half-time of 137Cs
in brown trout from Lake Trawsynydd, North Wales, (a potassium-deficient
lake receiving nuclear power effluents) was 500 days and the concentration
factor was near 40,000.
Cesium can be accumulated by fishes both from food and through water.
Cesium is chemically similar to potassium; thus waters with high potassium
levels such as the ocean inhibit cesium uptake, accounting for the wide
variety of concentration factors reported by various workers. Organism
size is inversely related to rate of cesium uptake or elimination probably
due to size-related metabolic differences. Although cesium has a relatively
low toxicity to humans, the isotope is very hazardous. Because a large
percentage of the cesium accumulated by fishes lodges in edible muscle
tissue, sport and commercial fisheries suspected to be contaminated by
radiocesium should be carefully monitored.
21
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SECTION IX
CHROMIUM
Chromium is used in electroplating, steelmaking, photography, and
some chemical syntheses. Although not as toxic as many metals, chromium
has been known to cause ulcers, skin lesions and cancer in humans (Berry
e_t al_. 1974). In water trivalent chromium exists as a complex, colloid,
or precipitate, depending on pH; hexavalent chromium is usually present
only as an ion (Knoll and Fromm 1960). Potential sources of chromium in
water include industrial wastes and nuclear effluents.
Chromium content was shown to increase with age in lake trout
(Salvelinus namaycush) collected from a New York state lake (long et al.
1974). Knoll and Fromm (1960) exposed rainbow trout (Salmo gairdneri^~to
2.5 mg £-1 hexavalent chromium in water for up to 24 days and measured
chromium uptake in various tissues. Some fish we're also exposed for only
12 days then placed in chromium-free water for 24 days to measure elimina-
tion. Pyloric caeca attained the highest concentrations of chromium
followed by gut, kidney and liver. Except for spleen and kidney, all
tissues lost chromium rapidly after exposure to freshwater conditions.
Results indicate that chromium is transported by the body to the gut where
it can be eliminated through the feces. Chromium administered to the gut
through a stomach tube was over 50 percent eliminated after one day and
none was distributed to other organs. This result implicates the gill
as the major route of chromium accumulation. Edible tissues did not
accumulate significant amounts of chromium.
In another study Kuhnert and Kuhnert (1976) measured chromium content
of rainbow trout gill, kidney, liver and intestine following 48 hours' in
vivo exposure to 2.5 mg Cr a~L as chromate. Kidney and gill accumulated
about four times as much chromium as either intestine or liver. Fromm and
Stokes (1962) found that rainbow trout took 10 days to reach whole body
equilibrium chromium concentration upon exposure to hexavalent chromium
(as chromate) levels below 0.01 mg Cr &"1. However, fish exposed to chromium
concentrations of 0.05 mg £~1 and higher continued to accumulate chromium
linearly in time until the test was terminated after 30 days. In a
laboratory study Buhler et_ aj_. (1977) analyzed two groups of rainbow trout
raised in two natural waters differing in chromium content. Trout contained
chromium levels in proportion to the chromium in their environment. Trout
exposed to 2.5 mg jr1 hexavalent chromium accumulated chromium rapidly
during the first day of exposure but did not accumulate appreciable chromium
during further exposures for up to 22 days. Apparently an equilibrium con-
dition was rapidly reached. Tissues having the highest chromium levels were
22
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spleen, kidney, gastrointestinal tract, gall bladder and opercular bone.
In goldfish (Carassius auratus) 51Cr was accumulated to the largest extent
in air bladder, kidney and head kidney (Hibiya and Oguri 1961). The marine
polychaete Nereis virens also accumulated chromium in proportion to exposure
level, demonstrating accumulation through both gut and epithelium (Raymont
and Shields 1963).
Shuster and Pringle (1969) exposed American eastern oysters (Crassostrea
virginica) to either 0.05 or 0.1 mg Cr £-1 for 20 weeks. At the termination
of the experiment oysters exposed to the two levels averaged about 6.0 and
11.0 yg Cr g"1 respectively. Comparatively, east coast oysters collected
from Maine through North Carolina ranged from <0.12 to 3.40 yg Cr g"1
(Pringle e_t a_l_. 1968). Chromium concentration factors for marine organisms
have been reported to approach 2000 for various planktonic forms, 500 in
shellfishes and 100 in crustaceans and fishes (Lowman et, al_. 1971).
Chipman (1967) measured chromium (as 51Cr) uptake by the marine poly-
chaete worm, Eermione hystrix. Orally ingested trivalent chromium was not
assimilated by the worms; however worms accumulated hexavalent chromium from
water. A concentration factor of 12 was attained after 19 days' exposure,
and worms were still accumulating chromium at the end of the test; uptake
was proportional to exposure concentration indicating that accumulation was
a passive process. Chromium elimination was from'two compartments each
accounting for about half of the initial burden. Biological half-times for
the two elimination phases were 123 and 4 to 8 days. It was suggested that
longer exposures to the metal would result in a higher percentage of the
accumulated chromium being present in the slowly eliminated compartment.
Some fishes are capable of attaining chromium levels nearly 100-fold
the concentrations of chromium in water; however, reports of the time re-
quired for these fish to reach equilibrium tissue levels of chromium vary
from one day to over 30 days. Apparently exposure level and some unknown
factors influence this relationship. What is clear is that fish rapidly
eliminate chromium upon return to freshwater following exposure. Thus,
fish exposed intermittently to high chromium levels would not experience
cumulative chromium uptake.
In fishes chromium is apparently accumulated from water through the
gills followed by transport via the blood to the various organs and tissues.
Eventually chromium reaches the gut where it is eliminated through the feces.
Because fishes accumulate relatively little chromium in edible tissues and
because chromium is low in toxicity to humans, consumption of chromium-
contaminated fish by humans should not result in toxicosis.
23
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SECTION X
COBALT
Cobalt is widely used as an alloy, a pigment for glassware and as a
binder for manufacturing tools (McKee and Wolf 1963). Cobalt is also used
in nuclear generated electrical power plants and may enter water in the
effluents from this industry. Cobalt dusts from refinery and alloy plants
have resulted in human poisonings characterized by dermatitis, gastro-
intestinal pain, vomiting and low blood pressure (Berry et_ al_. 1974).
However, trace amounts of dietary cobalt are essential to human health.
Brungs (1967) released 60Co along with several other radionuclides into
a pond containing a typical warmwater fauna. Following introduction cobalt
rapidly became associated with bottom sediments and suspended solids. Most
of the cobalt accumulated by pond organisms was present in soft tissues. In
a laboratory study, Nile catfisH (Clarias lazera) attained the highest levels
of 60Co in muscle, bone and gill (Ishak et_ al. 1977) but the whole body con-
centration factor (dry weight basis) was onTy 0.36. Gill attained higher
levels when 60Co was present in water rather than food.
Eggs of pike (Esox lucius), perch (Perca fluviatilis], and whitefish
(Coregonus lavaretus) were exposed to 60Co for up to 120 days (Kulikov and
Ozhegov 1975). Equilibrium concentration factors differed considerably
(-1 to -36) depending on fish species, life stage and incubation water
temperature. Uptake of cobalt by eggs was believed to be based on sorption
of cobalt on the egg surface and not on physiological and biochemical pro-
cesses inside the egg. Evidence for this was the fact that pike larvae
hatched from cobalt-exposed eggs were practically cobalt-free; also, the
length of time required to establish an equilibrium distribution of 60Co
between eggs and water was the same in all cases regardless of the concen-
tration factor. Eggs exposed to 60Co for two days then placed in cobalt-
free water until hatching eliminated cobalt rapidly. By the end of incuba-
tion, perch eliminated 80 percent, whitefish 57 percent and pike 40 percent;
the rate of elimination was faster at higher temperatures.
Amiard-Triquet and Amiard (1975) measured the transfer of 60Co through
a food chain comprised of diatom (Navicula sp.), bivalve (Scrobicularia
pla.no), shore crab (Carcinus maenas) and rat (Rattus rattus). Diatoms
accumulated substantial 60Co but the accumulation of 60Co by other organisms
was inversely related to trophic level. Rat accumulated highest 60Co
concentrations in liver, and crabs and bivalves had highest levels in
hepatopancreas. Similarly, Mathis and Cummings (1973) noted an inverse
relationship between trophic position and cobalt tissue levels among various'
24
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biota from the Illinois River; in this study fishes averaged 0.1 yg Co g"1.
In comparison, whole fish from the Danube River, Austria, averaged 0.3 yg Co
g"1 dry weight (Rehwoldt et al. 1975) while great lakes fishes averaged
0.022 to 0.042 yg Co g'1 "{Lucas ejt a]_. 1970) and eviscerated decapitated
New York lake trout (Salvelinus namaycush) averaged 0.043 to 0.081 yg Co g'1.
Cobalt concentrations have also been reported for some marine organisms.
Calico bass (Paralabrax clafhratus} collected off southern California con-
tained 0.012 to 0.052 yg Co g'1 dry tissue (Stapleton 1968); clams (Ensis
sp.), mussel (Mytilus sp.) and common shrimp (Crangon crangon} from several
locations along the Belgian coast averaged (in yg Co g'1 dry tissue)
0.028-0.105, 0.014-0.11 and 0.18-1.04 respectively (Bertine and Goldberg
1972). Pacific oysters (Crassostrea gigas] contained 0.10 to 0.20 yg Co
g'1 and American eastern oysters (Crassostrea virginiaa] ranged from 0.06
to 0.20 yg Co g"1 (Pringle ejt al_. 1968); and zooplankton collected near
Puerto Rico averaged 40 yg Co g'1 dry weight (Martin 1970).
Van Weers (1975) measured 60Co uptake and retention by the common
shrimp under a variety of exposure conditions. Shrimp readily accumulated
the isotope from both food and water. Decreasing the water temperature
from 15 to 5 C resulted in a slight decrease in cobalt uptake by the
shrimp. A considerable portion of accumulated cobalt was lost during
molting; the elimination process was comprised of two phases. With a 10 C
increase in water temperature, the biological half-times of the slow and
fast phases were reduced from 12.8 to 6.9 days and from 2.0 to 1.2 days,
respectively.
Although planktonic organisms accumulate considerable cobalt, higher
animals including fishes appear to accumulate very little. Upon entering
water, cobalt apparently tends to associate quickly with particulate matter
and sediments thereby becoming unavailable for accumulation by most organisms,
Because cobalt is an essential element, its toxicity is relatively low;
however, radiocobalt is more hazardous. Marine shellfishes, because of
their metals concentrating ability and because they live on or in the sedi-
ment, should be monitored in areas where high radiocobalt levels are
suspected.
25
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SECTION XI
COPPER
From the standpoint of human health, copper is relatively low in
toxicity compared to metals like mercury and cadmium, although prolonged
consumption of large doses has been known to cause emesis and liver damage
in humans (MAS 1973). The non-corrosive properties and low price of copper
make it highly desirable for use in electrical wire and water pipes. In
water, copper has been used as an algicide and is a common constituent of
acid mine drainage. Divalent copper ion (Cu2+) and its hydroxy complexes
are believed to be the toxic chemical species to fishes; and alkalinity
and pH are believed to be the major factors controlling copper speciation
(Chakoumakos 1977).
Goettl e_t aj_. (1972) determined baseline concentrations for copper in
various tissues from rainbow trout (Salmo gairdneri) collected from a re-
search hatchery with a pristine water supply. On a dry weight basis values
were (in ug Cu g"1)' opercular bone 7.3, eye 4.3, gill 4.9, intestine 9.6,
kidney 12.9 and muscle 1.7. McKim and Benoit (1974) measured copper levels
in gill, kidney, liver and muscle from brook trout (Salvelinus font-inalis]
previously exposed to copper in water from the egg stage through spawning.
Even the highest copper concentration employed (9.4 yg jr1) resulted in no
detectable copper accumulation in any of the tissues analyzed; however,
the copper levels used were considered quite low, since none of the
exposure levels adversely affected the trout. Using considerably higher
copper levels Benoit (1975) found that bluegill (Lepomis macrochirus]
exposed for up to 22 months accumulated copper at all concentrations 40
yg JT1 and above; this same level was the lowest concentration having an
adverse effect (decreased larval survival) on bluegill. This result
suggests that fishes may be adversely affected by copper if they are
attaining copper tissue levels exceeding natural background levels.
Brungs et^ a_l_. (1973) measured copper uptake by brown bullhead
(latalurus nebulosus) exposed to various copper concentrations in water
in hopes of. establishing an autopsy technique useful for confirming copper-
caused fish kills. No useful relationship was found; moreover, lethal
exposure preceded by subacute exposure resulted in higher tissue copper
levels than in fish having experienced only the lethal conditions. Bullhead
accumulated copper at all water concentrations equaling or exceeding 27 yg
Cu fc"1. Copper concentrations in liver and gill tissues most accurately
reflected the copper exposure conditions. Equilibrium concentrations were
reached in these tissues after 30 days' exposure; however, Goettl et al.
(1974) found that rainbow trout continued to accumulate copper in TTver
for up to 107 weeks; moreover, trout accumulated copper in liver after
26
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exposure to only 3 yg Cu x,-1 in water. Copper elimination by stone loach
(Noemacheilus barbatulus) was studied following short exposures to relatively
high copper concentrations in water (Solbe and Cooper 1976). Gill, eye,
vertebrae and muscle all lost copper rapidly, but liver tended to retain
copper. In the marine mummichog (Fundulus heteroclitus) the presence of
copper was shown to enhance cadmium accumulation (Eisler and Gardner 1973);
in addition, dead mummichog accumulated copper more readily than living
individuals.
Nehring (1976) suggested that it may be possible to detect instances of
intermittently acute copper pollution in streams by monitoring copper levels
in aquatic insects because some stream insects including the mayfly
Ephemerella grandis and the stonefly Pteronarays califoxmica were more re-
sistant to copper than fishes and because copper residue accumulation
reflected the insects' copper exposure history. In the isopod Asellus
meridianus copper was accumulated from both food and water, particularly
in the hepatopancreas (Brown 1977). The hepatopancreas was believed to
be an important storage site for copper, possibly helping avoid the accumula-
tion of copper at more sensitive sites.
In a food chain consisting of copper-enriched sediment, bacteria and
tubificid worms (Tubifexsp.), copper level increased with increasing
trophic level (Patrick and Loutit 1976)-. However, Windom et al_. (1973)
found that for several North Atlantic fish species, copper~Tevel was in-
versely related to trophic position. Similarly, Cross et a]. (1973)
observed no increase in copper content with age among bTuefish (Pomatomus
saltatrix) and morids (Antimora rostrata) collected off the North Carolina
coast. Marks (1938) analyzed California coastal organisms for copper
including various snails, mussels and an octopus. Polypus bimaculatus.
Copper concentrations increased with size (age) in the common terrestrial
snail Helix aspersa, decreased with size in the sea mussel Mytilus
californianus, and remained the same regardless of size in the octopus.
These species as well as the majority of assorted other species analyzed
contained from 1 to 10 yg Cu g"1. Martin and Flegal (1975) measured the
concentrations of copper and various other metals in livers from squid
(Loligo opalescens, Ommastrephes bartrami, Symplectoteuthis oualaniensis)
collected off southern California. Squid were able to concentrate copper
in their livers to incredibly high levels with some individuals attaining
15,000 yg Cu g"1 on a dry basis, representing a concentration factor of 2.1
million. Increased copper levels were highly correlated with increasing
levels of silver, cadmium and zinc. It was hypothesized that squid
actively accumulated copper for synthesis of their major respiratory
pigment, hemocyanin, and that other similar metals were accumulated in
the process.
Scott and Major (1972) measured copper uptake by the mussel (Mytilus
edulis) exposed to 0.3 mg Cu s,"1 for four days in a static seawater system.
Mussels accumulated copper for the first 22 hours but then began eliminating
copper with tissue returning to background levels after 48 hours. This loss
of copper resulted from the mussels' excreting large quantities of mucus,
thus rendering the excreted copper unavailable for reaccumulation. The loss
of copper by mussels during these experiments would probably not occur in a
27
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flow-through system where copper was continually being renewed in the solu-
tion. The marine polychaete worm (Nereis virens] accumulated copper in
laboratory experiments through both gut and epithelium, and uptake was pro-
portional to exposure level (Raymont and Shields 1963). Oysters (Crassostrea
virginica) exposed to 0.025 or 0.05 mg Cu i~l in seawater for 20 weeks
averaged about 700 or 1050 yg Cu g"1 of soft tissue respectively (Shuster
and Pringle 1969). In comparison, the same species collected from various
portions of the U.S. Atlantic Coast ranged from 6.83 to 517.4 yg Cu g"1
(Pringle e_t al_. 1968). High copper tissue levels caused the oysters to
take on a greenish tint. Martin et al_. (1977) measured copper levels in
red abalone (Haliotis rufescens) suspected to have been exposed to excessive
copper from the discharges of a California nuclear power plant. Copper was
believed to have leached from copper tubing in the condensing system during
a non-operational period. Only living red abalone were analyzed, although
over 1000 mortalities had been observed at an earlier date. Abalone con-
tained on the average 65 yg Cu g"1 in gill with values ranging from 48 to
78 yg Cu g-1. In addition, copper accumulation experiments were performed
on red and black abalone (Haliotis cracherodii] in the laboratory. The
gills of red abalone that died due to copper contained 62 to 185 yg Cu g"1,
whereas survivors contained 5 to 98 yg Cu g"1 in gill. Dead black abalone
ranged from 92 to 291 yg Cu q'1 in gill; survivors accumulated gill copper
levels of 12 to 116 yg Cu g, .„ For a given copper concentration in watej
black abalone averaged higher copper levels in gill than red abalone, but
black abalone were also more resistant to copper. Copper levels in water
near 56 yg Cu x,"1 resulted in both species attaining gill copper concentra-
tions that were acutely lethal to some individuals; the experimental
evidence suggests that copper could have been responsible for an abalone
kill observed in the field.
Copper is accumulated by freshwater and marine fishes and shellfishes
and by aquatic insects. There appears to be a good correlation between
the onset of copper accumulation above background levels and the development
of chronic symptoms in fishes. This relationship may prove useful for
detecting conditions capable of causing chronic copper poisoning in natural
waters. Although the reports of various workers vary considerably as to what
is the lowest copper concentration in water resulting in copper accumulation
by fish, these differences can probably be explained on the basis of how
the chemical characteristics of the different test waters influenced copper
speciation. Liver and gill tissues from fish most accurately reflect copper
exposure conditions with liver retaining copper the longest after cessation
of exposure. The copper content of stream insects may be a useful index for
detecting acute copper exposures after it is too late to measure the copper
content of the water. It is doubtful that even the highest concentration of
copper concentrated by fish could harm human consumers because copper is low
in toxicity to humans and does not tend to accumulate in the edible tissues
of fishes. Oysters and squid, however, could represent a problem in areas
of copper contamination due to their high enriching tendency.
28
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SECTION XII
IRON
Iron is the second most abundant metal in the earth's crust. It
enters natural waters from corrosion, steel pickling, mineral processing
and acid mine drainage (NAS 1973). Although iron is an essential element
and has a relatively low toxicity to humans, large doses have caused internal
hemorrhaging, necrosis of the stomach, intestine and liver, and pulmonary
congestion (Berry e_t al_. 1974). Iron(II) is readily oxidized to iron(III)
in most natural surface waters and a substantial fraction of this iron is
present in suspended form (Stumm and Morgan 1970).
Iron concentrations in freshwater fishes from various areas have been
reported. Lake trout, Salvelinus nconaijaush (eviscerated, decapitated
homogenate) of known ages from Lake Cayuga, New York, averaged 0.14 to 0.34
yg Fe g'1 (long e_t aj_.. 1974). On a dry basis whole bluegill (Lepomis
maaroohirus), blueback herring (Alosa aestivalis), brook silverside
(Labidesthes sioaulus] and chain pickerel (Esox niger) from a South Carolina
reservoir averaged 148.7, 130.9, 149.3 and 39.3 yg Fe g"1 respectively
(Giesy and Wiener 1977). Rehwoldt e_t al_. (1975) found 7.6 to 42.1 yg Fe g-1
in whole carp (Cyprinus aarpio) or whitefish (Albuxmus) from the Danube
River, Austria. The distribution of iron in Danube carp was 9 percent in
kidney, 70 in liver, 20 in flesh and 1 in bone (Rehwoldt ejt al_. 1976);
these percentages were not adjusted for iron in gill'. Mean concentrations
(yg Fe g"1 dry tissue) for the various tissues were: gill 14,597, kidney
2.49, liver 19.39, flesh 5.54 and bone 0.277. In comparison, calico bass
(Paralabrax clathratus), a marine fish collected near Catalina Island,
California, averaged 44 yg Fe g~! in dorsal muscle and 160 yg Fe g"1 in
liver on a dry weight basis (Stapleton 1968); and American eastern oysters
(Crassostrea virginioa) collected off the United States eastern seaboard
contained 30 to 238 yg Fe g"1, and clams contained 50-1710 (Pringle et al.
1968). None of these workers reported age-related increases in iron content.
Iron concentration factors have been determined for several marine and
freshwater organisms. Values (dry basis) include: 40 for soft tissues of
shrimp (Ensis ens-is} collected off the coast of Belgium (Bertine and Goldberg
1972), 14,400 for mixed zooplankton collected near Puerto Rico (Martin
1970), 1,840 for Lake Michigan benthos (Thomas 1975) and 10,000 and 1,000
for the soft parts of marine invertebrates and vertebrates respectively
(Krumholz et al_. 1957).
Iron is concentrated to a considerable degree by some marine organisms,
and fish accumulate high levels of iron in gill; the iron concentrations in
fish do not appear to increase with age. Because of the low toxicity of
iron to humans, iron in seafoods and freshwater fishes does not constitute
a hazard to human consumers.
29
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SECTION XIII
LEAD
Lead has long been known to cause poisonings in humans. Some his-
torians have attributed the decline of the Roman Empire to the Roman
practice of storing wine in lead-glazed pots. Early symptoms of lead
poisoning include anemia and behavioral problems, and advanced plumbism
is characterized by cramps, vomiting, kidney damage and neurological dis-
turbances (Berry ejt aj_. 1974). Important sources of lead in the environ-
ment include automobile exhaust, smelting smoke and lead base paints. Lead
mine runoff, outboard motor exhaust (Aronson 1971), highway runoff (Laxen
and Harrison 1977), snowmobile exhaust (Adams 1975) and atmospheric fallout
(Shukla and Lei and 1973) have all been shown to contribute significantly to
the lead content of some natural waters. However, most lead is probably
precipitated in natural waters due to the presence of carbonates and
hydroxides.
Chow e_t aj_. (1974) found that epidermis from various tuna fishes
including yellowfin tuna (Neothunnus macropterus), skipjack (Katsuwanus
pelamis), and albacore (Thunnus alalunga] contained nearly 10,000 times
as much lead as muscle tissue. Most of the lead present in epidermis was
associated with mucus. Dermis contained nearly 100-fold less lead than
epidermis. Thus, muscle tissue being analyzed for lead can easily be con-
taminated by mucus. Also revealed was the fact that much canned tuna is
contaminated over 1000-fold with industrial lead from the factory. Prepared
tuna samples of known lead content were sent to various laboratories for
independent lead analyses; analytical results confirmed that most analysts
could not accurately measure the lead content of fish. Results also suggest
that current analytical techniques are not sensitive enough to measure
natural levels of lead in marine and freshwaters. These findings should
be taken into account when interpreting the following reports.
Varanasi and Markey (1977) studied lead accumulation in rainbow trout
(Salmo gairdneri} skin and examined the influence of calcium concentration
on lead accumulation from water. Most of the lead in skin was associated
with scales. After six weeks in lead-free water fish retained over 70
percent of the lead they had accumulated. Calcium markedly decreased lead
accumulation on skin suggesting that lead might in turn interfere with the
ability of fish to accumulate calcium for bony structures.
Merlini and Pozzi (1977a) measured lead uptake in pumpkinseed sunfish
(Lepomis gibbosus] exposed to 203Pb at pH 6.0 and 7.5. Fish at the lower
pH accumulated three times as much lead as fish kept at pH 7.5. Gill,
30
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liver and fin accumulated the most lead and muscle the least. The authors
attributed the increased lead uptake at low pH to the increasing concentra-
tion of divalent lead with decreasing pH. In another experiment Merlini
and Pozzi (1977b) found a direct correlation between lead accumulation by
pumpkinseed sunfish and the concentration of ionic lead in water at various
concentrations of total lead. Results suggest that the conditions existing
in the majority of natural waters render most lead unavailable for accumula-
tion by aquatic animals.
Holcombe et_ a_l_. (1976) exposed brook trout (Salvelinus fontinaHs} to
various lead concentrations over three generations. Kidney and gill accumu-
lated the highest concentrations of lead followed by liver; muscle accumulated
very little lead. Based on the results of these experiments the Maximum
Acceptable Toxicant Concentration (MATC) was concluded to be between 58 and
119 yg Pb xr1 total lead; the incidence of spinal scoliosis was the determin-
ing factor. Trout exposed to 119 yg Pb £-1 accumulated over 100 yg Pb g"1
(on a dry basis) in gill, liver and kidney after 38 weeks. The authors
postulated that the equilibrium tissue levels (-50 yg Pb g'1 for liver and
-180 for kidney) for fish exposed to 119 yg Pb x,"1 could be used as an index
to detect sublethal chronic lead damage in nature. Gill, liver and kidney
lost about 75 percent of their accumulated lead after fish spent 12 weeks
in a lead-free environment.
Adams (1975) exposed groups of caged brook trout to water in a pond
having a history of heavy snowmobile use the previous winter. Snowmobile
use on the pond was controlled and trout were held in the pond for three
weeks following ice-out. Lead content of the water increased from 4.1 yg
XT1 in the falls of 1972 and 1973 to 88 and 135 yg JT1 in the respective
springs following ice-out. During these same years control fish averaged
0.37 and 0.64 yg Pb g"1 while caged fish contained 5.82 and 5.66 yg Pb g'1.
Trout kept in melted snow containing snowmobile exhaust accumulated lead in
proportion to the concentration of exhaust. Of the various tissues analyzed,
gut had the highest lead content.
Pagenkopf and Neuman (1974) measured the lead content of various cold-
water fish species taken from a stretch of the West Gal latin River, Montana,
paralleling a highway with a moderate traffic flow. Lead values in these
fishes were not significantly different from the lead content of fishes
from areas with no known source of lead pollution. In another survey,
Pakkala et_ a_l_. (1972) measured the lead content of decapitated, eviscerated
fish taken from various regions of New York state. Most fish contained
between 0.3 and 1.5 yg g-1 of lead. No trend was apparent between age and
lead content in lake trout (Salvelinus namaycush] taken from Lake Cayuga.
The lack of any apparent trend could be due to the fact that tissues known
to concentrate lead were discarded from the samples.
In laboratory experiments, isopods (Asellus mep-i.di.anus) accumulated
lead from both food and water with hepatopancreas attaining the highest
concentration (Brown 1977). Three different natural isopod populations
were used during the experiments and it was found that individuals from
the most lead-tolerant population also accumulated the most lead. Suggest-
ed mechanisms for this tolerance included improved ability to store lead
31
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and a better lead detoxification system. Interestingly, sulfur was detected
at much higher levels in the tolerant group suggesting perhaps that toxicity
was avoided due to sulfhydryl binding of the metal.
Lead accumulation by marine organisms has also been studied. Gajewska
ejt ajL (1976) surveyed saltwater fishes collected from the South Baltic and
North Atlantic, and freshwater fishes from Poland, for their lead content. :
Saltwater fishes ranged from 0.020 to 1.330 m'g Pb kg'1 and freshwater fishes .
ranged from 0.020 to 2,640 mg Pb kg'1. Kauranen and Jarvenpaa (1972)
measured the biological half-time of lead and polonium in various marine
organisms including Mytilus edulis, Mesidotae entonom, Gammarus zaddaahi
and Harmothoe sarsi in an attempt to explain the fact that the Po/Pb ratio
is greater than unity in many marine organisms. All organisms except
Harmothoe displayed an initial fast elimination phase for both metals
followed by an extended period of slow elimination. Lead had a considerably
longer half-time than polonium in all organisms tested, particularly the
mussel Mytilus sp. The polychaete Harmothoe had the longest half-time for
polonium (180 days). Because lead has a longer half-time than polonium, the
high polonium-to-lead ratio in marine organisms must be due to a preferen-
tial uptake of polonium.
Stewart and Sehulz-Baldes; (;1976), fed abaTone (Haliotis rufesaens) a
diet of lead-treated brown algae'{Egvegia laewigata) for three to six
months. Lead accumulation by abalone was directly related to the concen-
tration of lead in their diet. Kidney and digestive gland accumulated the
highest levels of lead but edible muscle (foot) accumulated very little
lead. Tissue burdens of up to 21 yg Pb g"1 had no adverse effects on the
abalone.
Chow £t a]_. (1976) were able to correlate the lead content in two
species of marine mussels (Mytilus ealifornianus and M. edulis) with the
degree of human activity in the area from which they were collected. The
highest concentration found was 4.2 yg Pb g"1, and gill tissue contained
the highest lead level among organs. Exposure of American eastern oysters
(Crassostrea virginiaa) in seawater to 0.1 or 0.2 mg Pb s,"1 for 10 weeks
resulted in the development of an emaciated condition (Shuster and
Pringle 1969). Ten-week exposures to 0.025, 0.05, 0.10 or 0.20 mg Pb jr1
resulted in oysters averaging 35.1, 57.6, 102.9 and 276.8 yg Pb g"1 respec-
tively, representing concentration factors ranging from 1030-1400. Oysters
collected from the eastern coast of the United States contained <0,12 to
2.29 yg Pb g"1 (Pringle et al. 1968). The Canadian Food and Drug Director-
ate has established 2 yg g-^as the maximum concentration of lead allowable.
in fish food (Adams 1975). This level could therefore be attained by oysters
after exposure to less than 2 yg Pb JT1. This is not an unlikely possibil-
ity since the average lead content of major U.S. rivers has been reported
to be 23 yg £-1 (Kopp and Kroner 1970).
Lead may enter natural waters through a variety of sources. Upon
entering water most lead is precipitated as carbonates or hydroxides;
however, decreasing pH increases the availability of divalent lead, the
principal form accumulated by aquatic animals. Many values reported for
lead in fish tissue could be in error due to contamination from mucus.
32
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Fishes accumulate very little lead in edible tissues; however, oysters and
mussels are capable of attaining unacceptably high lead concentrations in
edible portions after exposure to very low levels of lead in water. Based
on this information, fishes are probably not a major source of lead in the
human diet but shellfishes should be monitored closely. Calcium decreases
lead accumulation by fishes and lead may inhibit calcium accumulation and
deposition. Lead levels in fish livers exceeding 50 yg Pb g"1 and fish
kidney above 180 yg Pb g-1 may indicate a history of unacceptable lead
exposure.
33
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SECTION XIV
MANGANESE
Manganese ores are common in nature but the pure element does not exist
(McKee and Wolf 1963), Metallic manganese is used as an alloy in steel, and
manganese salts are extensively used in inks, dyes, ceramics, matches, fire-
works, batteries and paints (NAS 1973). Manganese has a low toxicity to
humans but poisonings have occurred from excessive exposures to the oxides
of manganese in manganese plants (Berry et_ al_. 1974); symptoms include head-
ache, weakness of muscles, tremors, reduced mental capacity and increased
susceptibility to pneumonia and other respiratory diseases. Manganese may
enter water from industrial outfalls and as a component of acid mine drain-
age. Although manganese chlorides, nitrates and sulfates are quite soluble
in water, its carbonates, oxides and hydroxides are relatively insoluble
(Kopp and Kroner 1970). Manganese has been reported to be one of the least
acutely toxic metals to fishes (D'oudoroff and Katz 1953).
Orally administered 5l+Mn was accumulated almost exclusively in the
bone of plaice (Pleuronectes platessa) (Pentreath 1973). Plaice concentrated
manganese from water 1650-fold. The elimination of manganese accumulated
from water was divided into two phases having biological half-times of 3.9
and 329.2 days. The slower phase accounted for 80 percent of the initial
body burden. Intraperitoneally injected manganese was more readily eliminated;
mean half-times for the two phases of elimination were 5.6 and 166.3 days.
Various workers have surveyed freshwater and marine fishes for their
manganese content. Headless, dressed, homogenized samples of lake white-
fish (Coregonus clupeaformis) and northern pike (Esox luoius) from Canadian
lakes contained from 0.66 to 3.16 yg Mn g'1 (Uthe and Bligh 1971). Similarly
prepared samples of lake trout (Salvelinus namaycush] from Lake Cayuga, New
York, contained 0.013 to 0.052 yg Mn g"1 (Tong et al_. 1974). No correlation
existed between lake trout age and manganese tissue concentration. Abdullah
el a_l_. (1976) found that brown trout (Salmo trutta) and Atlantic salmon
smolts (Salmo salar) collected from British waters contained high manganese
concentrations in their scales, with most individuals containing from 30 to
100 yg Mn g"1 in scale. Several estuarine fishes collected near Beaufort,
North Carolina, averaged 19 to 35 yg Mn g"1 dry weight (Cross and Brooks
1973). Bluefish (Pomatomus saltatrix] and morids (Antimora rostrata)
collected off the North Carolina coast averaged about 0.2 yg Mn g"1 in
muscle (Cross et^ al_. 1973); and calico bass (Paralabrax clathratus) from
the California coast averaged 0.5 yg Mn g-1 of dry dorsal muscle tissue.
Similar to reports for freshwater fishes, manganese concentration was not
related to fish size. American eastern oysters (Crassostrea virginica)
34
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collected at various locations from Maine to North Carolina contained 0.14
to 15.00 yg Mn g-1 (Pringle ejt al_. 1968). Marine gastropods (Thais lapillus
and Littorina Uttorea) collected off the coast of Wales were found to contain
over 80 percent of their body burden of manganese in gonad and digestive gland
(Ireland and Wootton 1977), and Bryan (1971) has noted high manganese levels
in the hepatopancreas of marine Crustacea. These results suggest that food
may be a major source of manganese to these organisms.
Patrick and Loutit (1976) have shown that tubificid worms (Tubifex sp.)
can accumulate manganese from their diet, and Thomas (1975) has reported that
lake benthos can concentrate manganese 3700-fold. Thus invertebrate food
organisms may be important sources of manganese to higher organisms.
Manganese has been detected in marine and freshwater fishes and has been
shown to be accumulated via the food chain by marine and freshwater inverte-
brates. However, manganese appears to be a relatively non-hazardous element
in most waters due to the low toxicity of manganese to humans and to aquatic
life and the insolubi-lity of manganese under most natural conditions. Further
investigations are, however, needed to relate manganese tissue residues in
aquatic organisms to manganese toxicity under those conditions, such as acid
mine drainage, which increase the solubility of manganese.
35
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SECTION- XV
MERCURY
The mercury literature has been extensively reviewed by Lofroth (1970),
Ackefors (1971), Study Group on Mercury Hazards (1971), Wojtalik (1971),
D'ltri (1972), Skerfving(1972)", Sana (1972), Gavis and Ferguson (1972),
Kojima and Fujita (1973), Lofroth (1973), Peterson et al_. (1973), Neville
and Berlin (1974), Jernelb'v et aV. (1975), Stopford and Goldwater t!975)!,
and Doi and Ui (1975). Because of the breadth of the mercury literature
and because mercury has been thoroughly reviewed by many workers since
1970, only those papers published subsequent to the most recent review will
be considered in detail here. However, a few of the most important earlier.
findings are briefly summarized.
The worldwide concern over mercury in the aquatic environment is re-
flected by the fact that the Winamata Bay arid Agano River, Japan, mercury
poisonings resulting from human"consumption of contaminated fishes and
shellfishes are now almost common household knowledge. The Study Group on
Mercury Hazards (1971) has described the human health aspects of methy!-
mercury poisoning including clinical symptoms and the major sources of
mercury to the environment. Victims suffer from paresthesia, a taxi a-,
deafness, blindness and deterioration of the central nervous system followed1
by death. Most mercury in the environment results from the chlor-alkali
industry, the pulp and paper industry, seed fungicide treatment, burning
of fossil fuels, mercurial catalysts used in industry and natural weathering
processes. In the United States and Canada the most severe cases of con-
tamination to aquatic environments have been attributed to the chlor-alkali
and pulp and paper industries.
Most of the mercury found in fish tissue, particularly edible portions,
has been shown to be methylmercury with few exceptions (Uthe e_t al_. 1973;
Westoo 1973; Laarman ert al_. 1976; Hildebrand et^ al_. 1976). ' Matsumura et a_K
(1975) have shown that liver preparations from a variety of freshwater and
marine fishes are capable of converting mercuric ion to methylmercury i_n_
vitro. However, in view of the fact that exposure of fishes to mercuric
ion in water results in mostly inorganic mercury'-in-their tissue (Hannerz
1968; Cox et_ aj_. 1975) it is likely that the high levels of methylmercury. :
found in fishes in nature result from exposure.to methylmercury in their
environment.
Bacteria common to most natural waters have been proven capable of con-
verting many mercury compounds to methylmercury (Jensen and Jernelb'v 1969;
Wood
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mercury compound entering water may become a bioaccumulation hazard if the
environmental conditions are favorable for methylation. Other microbial
conversions of mercury have also been reported. Iverson et_ al_. (1975) have
shown that certain bacteria, primarily Pseudomonas sp., are capable of
transforming mercuric ion and phenylmercuric acetate to volatile elemental
mercury, and Spangler et_ al_. (1973) have described a process whereby methyl-
mercury is demethylated. Thus under certain conditions the most noxious
forms of mercury can be converted to less toxic forms.
Bisogni and Lawrence (1975) described the influences of inorganic
mercury concentration, availability of inorganic mercury, pH, microbial
activity and redox potential on mercury methylation rates. In general,
more methylmercury is produced when more inorganic mercury is present.
Chemical agents which precipitate mercury, such as sulfide, reduce the
availability of mercury for methylation, but only when present in large
quantities. At neutral pH the primary product of mercury methylation is
monomethylmercury. Methylation can occur under both aerobic and anaerobic
conditions, but more mercury is produced when more bacteria are present.
Hence, highly organic sediments which favor bacterial growth have a higher
methylation potential than inorganic sediments. The authors suggested
several methods of decontaminating mercury-laden aquatic environments in-
cluding (1) addition of strong complexing agents, (2) elimination of nutri-
ent inputs, and (3) reducing the amount of inorganic mercury available in
the sediment by dredging, covering, or application of a removable mesh
having a high mercury affinity. All of these methods would be extremely
costly. In another study Shin and Krenkel (1976) quantified the influences
of temperature, BOD, pH, chloride ion concentration and mercury ion concen-
tration on the methylation process and subsequent methylmercury accumulation
by mosquitofish (Gambusia affinis] or guppy (Poecilia reticulata]. Fish
accumulated more mercury as temperature and mercury content of sediment
increased. A chloride ion concentration of 200 mg &'1 and a pH near neutral-
ity were ideal for methylation with variation in either direction resulting
in reduced methylation. BOD's in the range 8-800 mg jr1 did.not influence
mercury accumulation. This last result is inconsistent with earlier find-
ings showing that conditions favoring bacterial growth enhanced methylation.
Demethylation of mercury was observed to occur when methylmercury levels
became excessive.
Ramamoorthy et_ al_. (1977) measured the uptake of mercury from water
by both bacteria and sediment. The bacterium Pseudomonas fluorescens and
the sediment (Ottawa River sediment, mostly kaolinite and illite) were sus-
pended in a mercury-spiked solution of Ottawa River water. Bacteria accumu-
lated mercury much more rapidly than sediment, taking up nearly 20-fold as
much mercury as sediment after 72 hours. Mercury loss from the system during
the experiment was attributed to the bacteria converting divalent mercury to
the volatile Hg°. This loss did not occur in water systems containing no
bacteria.
Kudo (1976) exposed guppies to water over a bed of 203Hg-enriched
sediment (1.0 yg Hg g-1) and measured the guppies1 mercury uptake. Mercury
uptake from water by the guppies was compensated for by increased mobiliza-
tion of mercury from sediment into water. The half-life of mercury in the
37
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sediment under these conditions was estimated to be 12-20 years. Over half
of the mercury present in the fish was organic, suggesting that conditions
were such that mercury was being methylated. In another study with inorganic
mercury Tsai et al. (1975) exposed fathead minnows (Pimephales promelas] and
emerald shiners ~(Wotropis atherinoides) to various concentrations of mercuric
chloride in water and measured the influence of pH on accumulation. Mercury
uptake increased as pH decreased, increasing sharply at pH values below 7.0.
Nearly 50 percent of all the mercury in the fish was associated with external
mucus. The decreased accumulation of mercury at high pH values was believed
to result from the increased formation of less reactive mercury hydroxide
complexes. The presence of HPOi42~ was also believed to inhibit mercury
accumulation, whereas the presence of sulfide increased mercury uptake.
Similarly, the presence of iodide and bromide increased mercury accumulation
by factors of 18 and 6 respectively. The authors suggested that more readily
accumulated mercury-halide or mercury-sulfide complexes were formed.
Communities of animals including snails, tadpoles, several species of
insects and mosquitofish were exposed to mercuric ion in artificial streams
(Cox e_t aj_. 1975). Mercury content of the organisms was related to habitat
and trophic level with carnivores and bottom dwellers having higher mercury
levels than herbivores and species living in the water column. Over 80 per-
cent of the mercury present in the organisms including the mosquitofish was
inorganic mercury.
Similarly, Kramer and Neidhart (1975) measured mercury uptake and
elimination from water in guppy using inorganic mercury and methylmercury
and found that methylmercury was more readily accumulated and retained than
inorganic mercury and that uptake rate increased with exposure level. Half-
time for methylmercury was 70 days, a much .lower value than that reported by
other workers. These findings support the hypothesis that inorganic mercury
is not the major source of mercury to fish in most natural environments.
Ruohtula and Miettinen (1975) measured uptake and elimination of 203Hg-
labeled methylmercury In rainbow trout (Salmo gaivdneri) following a single
dose injected into the stomach or exposure through the water. The biologi-
cal half-time ranged from about 200-500 days. Elimination time was inversely
related to water temperature. Miettinen (1975) discussed the biological
half-times of various mercury compounds in the mussel (Pseudanodonta
oomplanata] and in rainbow trout. In the mussel half-times for inorganic,
phenyl- and methylmercury were 23, 43 and 100-400 days respectively. In
rainbow trout half-times for methyl-, ethyl- and propylmercury were 346,
119 and 233 days respectively. Half-times decreased with increasing tissue
burden. Orally administered methylmercury was retained longer than methyl -
mercury accumulated from water. Smith e_t al_. (1975) compared the uptake
patterns of several mercury compounds including methylmercury, inorganic
mercury and phenylmercuric acetate by the freshwater clam Anodonta grandis.
All of the mercury compounds were readily accumulated but only methylmercury
was significantly retained by clams following their transfer to mercury-free
water. After exposure was terminated, methylmercury redistributed within
the organism so that foot increased in concentration, gill rapidly decreased,
and liver remained about the same. Surprisingly, temperature did not sig-
nificantly influence rate of uptake.
38
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Laarman et_ aj_. (1976) transferred yellow perch (Pevca flavescens] and
rock bass (Amblovlites rupestris) from mercury-contaminated Lake St. Clair
(midwestern U.S.) to essentially mercury-free earthen ponds. After two
years in the mercury-free environment, all of the reduction in the mercury
content of these fish could be accounted for by growth dilution.
Heisinger and Green (1975) exposed the eggs of the Japanese medaka
(Oryzias latipes) to various mercuric ion concentrations in water. Concen-
trations exceeding 15 yg Hg JT1 resulted in significantly reduced survival.
The observed toxicity resulted from hemolysis of the red blood cells.
Calabrese eit aJL (1975) examined the gill and blood uptake of mercury in
winter flounder (Pseudopleuvonectes ameriaanus) exposed to 5 or 10 yg Hg
ji"1 in water for 60 days. Mercury averaged 20.6 yg g"1 in gill and 2.9 in
blood for the fish exposed to 5 yg XT1 and 42.8 yg g-1 in gill and 3.8 in
blood for the fish exposed to 10 yg Hg &"1.
Giblin and Massaro (1975) studied the role of blood in the accumulation
and transport of methylmercury in rainbow trout; they found that hemoglobin
was the major site for methylmercury binding in blood, containing almost 95
percent of the methylmercury present. The rainbow trout hemoglobin molecule
was found to have four reactive -SH groups per hemoglobin molecule (compared
to two for humans), accounting for methylmercury's high affinity for hemo-
globin. Experiments showed that the binding of methylmercury to hemoglobin
was reversible and that even methylmercury injected into the trout as methyl-
mercury-S-cysteine eventually became bound to hemoglobin. These results
suggest that methylmercury bound to red blood cells can be transferred to
other tissues and organs and that red blood cells can also receive methyl-
mercury bound to other proteins. The rate of methylmercury transport in
and out of red blood cells was dependent on the concentration of -SH groups
on both sides of the cell membrane.
Fromm (1977) studied several physiological aspects of mercury accumula-
tion by rainbow trout using both 203HgCl2 and CH3203HgCl. Gill was found to
be the major site of mercury accumulation from water as opposed to gastro-
intestinal tract (swallowed water) or skin. Methylmercury was accumulated
far more readily than inorganic mercury, but inorganic mercury bound to gill
mucus over 14 times more readily than organic mercury. This difference
was believed to be due to the greater lipid solubility of methylmercury
thus allowing its entry across a cell membrane comprised primarily of lipid.
Exposure for up to 12 weeks to 10 yg Hg JT1 as methylmercury did not sig-
nificantly alter the concentration of plasma electrolytes including Na ,
K+, Cl", Ca2+ and Mg2"1"; however, an unexplainable increase in hematocrit
was noted. Oxygen consumption was unaffected by exposure.
Olson e£ al_. (1975) exposed fathead minnows to concentrations of methyl-
mercury in water ranging from 0.018 to 0.247 yg Hg i,"1 and measured whole
body levels after 48 weeks' exposure. Uptake was not proportional to expo-
sure concentration but increased with concentration. Fish exposed to the
lowest methylmercury level attained concentrations nearly three times the
FDA action level (0.5 yg Hg g"1). and minnows receiving the highest exposure
concentration exceeded the FDA level nearly 22-fold. In another chronic
toxicity study McKim et a_l_. (1976) exposed brook trout (Salvelinus fontinalis)
39
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to various methylmercury concentrations in water over three generations and
found that fish attained mercury concentrations in edible tissues exceeding-
the FDA guideline at exposure levels (as low as 0.03 yg Hg £"J) having no
adverse effects on growth, reproduction or survival. These findings suggest
that water quality standards should be based on a concentration of methylr
mercury in water which will provide protection for human consumers of fish.
Hartung (1976) pooled the data of previous workers to construct a model
of methylmercury accumulation from water. Uptake was found to conform to
zero-order kinetics during the initial uptake phase. The relationship
between water temperature and methylmercury accumulation rate for a given
methylmercury exposure was direct and also nearly linear. Experiments per-
formed at different laboratories with similar test species and at similar
temperatures agreed quite well.
Methylmercury is also readily accumulated by both fish and mammals
through their diets. Wobeser (1975) fed groups of rainbow trout finger!ings
diets containing from 4 to 24 yg Hg g"1 as methylmercury for 105 days. No
mortality was attributed to methylmercury even though some fish accumulated.
as much as 30 yg Hg g"1. Fish at the highest exposure level suffered from
minor gill hyperplasia. Scherer e_t al_. (1975) fed walleye (stizostedion
vitreum vitreum] a diet of shredded northern pike (Esox lupius] collected
from mercury-contaminated Clay Lake,'Ontario, and mea-sured mercury accumula-
tion in various tissues as well as the locomotor response of exposed fish.
Lens accumulated extremely high concentrations of mercury (over 200 yg g"^)
and exposed fish suffered from increased mortality and decreases in growth,
locomotor activity, coordination, and response, to light. Considerably less
fat was deposited in livers of mercury-fed fish as compared to controls.
Mink (Mustela visen] fed a diet of fish for 145 days containing mercury
concentrations approaching the FDA action level accumulated mercury levels
as high as 7.8 yg g'1 in liver, 6.5 in kidney and 8.3 in brain with no
adverse effects (Wobeser e_t al. 1976).
Suzuki _et al_. (1976) examined the socio-economic factors governing
the fish-eating habits and subsequent mercury accumulation by residents of
several small Japanese islands. The mercury content of both hair and blood
from islanders was correlated with the frequency of fish consumption and the
mercury content of the fish consumed. Factors governing the availability of
fish influenced the frequency of fish consumption. In another study con-
cerning mercury in the diets of humans Smith and Armstrong (1975) analyzed
the mercury levels in various dietary components of Northwest Territory
natives (Inuits) as well as in Arctic canines. Both bearded seals
(Erignathus barbatus] and ringed seals (Phoca hispida hispida] were, found
to contain exceedingly high levels of mercury in their livers. In addition',
liver contained high selenium levels. Most of the mercury present in seal
livers, unlike the case for fish, was inorganic suggesting a demethylation
process by this organ. Arctic char (Salvelinus alpinus), caribou (Pangifer
tarandus], Arctic fox (Alopex 'lagopus) and wolf (Canis lupus] contained
only modest mercury levels. However, sledge dogs (Canis familiar-is], which ,
feed primarily on seal, contained' extremely high mercury levels. Since the
Inuits1 diet consists primarily of caribou and Arctic char for most of the
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year and seal for only a short time, there appears to be no immediate
hazard; a problem could develop should seal become a more important dietary
constituent.
Conflicting reports exist in the literature regarding the relative
importance of food and water as sources of mercury to fishes. The Swedish
workers Fagerstrom and Asell (1976) insist that mercury uptake from water
via the gills accounts for most of the mercury present in fishes, but most
other reports show food to be a more important source. Norstrom et a!.
(1976) modeled methylmercury uptake by Ottawa River yellow perch deriving
coefficients for the various factors influencing methylmercury accumulation
from the literature and from their own laboratory experiments. Earlier work
had shown that 80 percent of the methylmercury present in food and 12 per-
cent of that passing over the gills was accumulated by the fish. Elimination
was described as a function of body weight and methylmercury body burden.
If the coefficients in the model are correct, then about 40 percent of the
methylmercury present in Ottawa River yellow perch was derived from the
water and 60 percent from their food. Experiments conducted by Terhaar et_
al. (1977) demonstrated that fathead minnows accumulated more mercury when
their food source (Daphnia magna) was raised in the test water. Suzuki and
Hatanaka (1974) estimated the percentage of methylmercury in young yellow-
tail (Seriora quinqueradiata) attributable to their food, based on the
relationship between food consumption rate and growth rate and the effi-
ciency of methylmercury extraction from food. Their estimates suggested
that food accounted for almost all of the mercury present in young yellow-
tail; however, the efficiency of methylmercury extraction from food was
based on laboratory experiments during which yellowtail were fed anchovies
(Engraulis japonica) which had been exposed previously to methylmercury-
dosed seawater for a short duration. Conceivably, longer exposures to
lower mercury concentrations, such as exist in nature, would result in a
body distribution of mercury in the food organism that would decrease
mercury's availability to a predator fish.
Many field investigations have been conducted during which various
workers have collected numerous freshwater and marine organisms and analyzed
them for their mercury content. In the United States Kelly ert al_. (1975)
measured the mercury concentrations found in walleye from several Michigan
lakes and compared these to values obtained from museum specimens collected
from the same lakes 40 years earlier. In comparing fish from seven collec-
tion sites, walleyes from three lakes increased in mercury, but specimens
from the other four sites decreased or remained the same. Anderson and
Smith (1977) measured the mercury levels in fish from an Illinois lake
located downwind from a coal-fired electrical power plant emitting large
amounts of mercury into the atmosphere. Fish were found to contain unusually
low concentrations of mercury compared to other Illinois lakes with no known
source of mercury, suggesting that conditions existing in the lake were act-
ing to suppress mercury accumulation by the fish; no hypotheses were
suggested. In a similar study, Aronson ejt al_. (1976) compared the muscle
mercury levels in fish from three Ohio lakes including industrialized Lake
Erie and two less industrialized lakes. Of the species analyzed, carp
(Cyprinus carpio] contained almost twice as much mercury as other species
from the non-industrialized lakes, but Lake Erie carp had the same average
41
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mercury content as coinhabitors. This discrepancy was believed to result
from a difference in the nutrient status of the two systems with Lake Erie
being more oligotrophic than the other lakes.
Hildebrand ejt al_. (1976) measured total mercury and methylmercury
levels in fishes and benthic fauna collected from the Holston River,
Virginia, at various distances downstream from the waste disposal ponds
from an abandoned chlor-alkali plant. Mercury concentrations were highest
in fish collected immediately below the pond (within two miles), but fish
collected as far as 80 miles downstream exceeded the FDA guideline. Nearly
90 percent of the mercury in fish and 50 percent of that in benthic inverte-
brates was methylmercury.
The mercury content of largemouth bass (Micropterus salmoides] from
three South Carolina reservoirs was correlated with trophic stage of the
reservoir (Abernathy and Cumbie 1977). Newer reservoirs were oligotrophic
in character and contained bass with higher mercury levels than bass from
older, more eutrophic reservoirs. The lower pH, higher dissolved oxygen
content, and lower alkalinity of the oligotrophic reservoir were believed
to enhance microbial methylation of mercury and subsequently promote mercury
accumulation by fish. Freshwater fish from various other South Carolina
water bodies have also been surveyed for their mercury content (Koli et al.
1977). Some northern pike and mudfish (Amia calva] exceeded the FDA guide-
line level but most fish contained permissible amounts. Kidney, liver and
muscle contained higher mercury levels than other tissues. In another
southern United States study Crockett e_t al_. (1975) measured the mercury
concentrations.in commercially grown channel catfish (letalurus punetatus}
collected from various catfish farms in Arkansas and Mississippi. Mercury
levels were very low, averaging 0.05 yg Hg g"1 with none of the fish analyzed
exceeding the FDA guideline. Cumbie (1975) found that mercury concentra-
tions in muscle tissue from fishes collected from the Suwanee River in
Georgia exceeded the FDA guideline. Hair samples from fish-eating mammals
(otter, Lutra canadensis , and mink) collected from the same area were found
to contain up to 68 yg Hg g"1 on a dry basis. These high mercury levels
in mammals were believed to have been accumulated via the food.
In the western United States Benson et^ al_. (1976) looked at the mercury
content of channel catfish and smallmouth bass (Micropterus dolomieui) from
the Snake River, Idaho. Most bass three years and older and catfish seven
years and older exceeded the FDA guideline, with bass attaining higher
mercury levels than catfish. Similarly, Richins and Risser (1975) examined
the mercury levels found in fish and crayfish from various areas of the
Carson River watershed in Nevada. Intensive gold and silver mining in the
drainage during the 1800's implicated this area for mercury contamination.
The survey revealed that edible tissues from some fishes exceeded the FDA
guideline; most notably, white bass (Roeeus cfoysops) from Lehontan
Reservoir averaged 1.3 yg Hg g"1. Potter ert a]_. (1975) reported on the
mercury content of various tissues from fishes and invertebrates collected
from Lake Powell near Page, Arizona. Interestingly, muscle contained the
highest mercury level of any tissue in most species: walleye, largemouth
bass, carp, black crappie (Pomoxis nigvomaculatus], and flannelmouth sucker
(Catostomus latipinnis]; however, liver, kidney, heart, spleen, stomach,
42
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brain and gill all exceeded muscle mercury levels in rainbow and brown trout
(Salmo trutta]. Apparently, modes of uptake, retention and elimination vary
among species. Factors which were believed to influence the observed levels
of mercury in plants and animals at different trophic levels included age,
surface area, metabolism, habitat and activity.
Various workers have also examined the mercury concentrations found in
organisms from foreign countries. Annett e_t al_. (1975) measured the mercury
content of muscle tissues from fish and waterfowl collected from the Ball
Lake area of the Wabigoon-English River system of Ontario, Canada. Ball
Lake is downriver from Dryden, Ontario, a town supporting a large paper mill
and chlor-alkali manufacturing facility. Both fishes and waterfowl were
found to be highly contaminated. The average mercury content in fishes
ranged from 0.51 to 13.54 yg Hg g"1 depending on species and sampling loca-
tion; waterfowl breast tissue ranged from 0.62 to 8.36 yg Hg g'1. All of
the waterfowl and 95 percent of the fish exceeded the FDA guideline, most
by several orders of magnitude; mercury levels in fish were near those re-
ported for Minamata Bay.
Renzoni and Bacci (1976) collected freshwater mussel (Vnio off.
elongatulus) from a river system located downstream from a large cinnibar
mine and refinery in Italy. The concentration of mercury in adductor
muscle was linearly related to mussel size, with digestive gland and gill
tissues containing the highest concentrations of mercury. Half-time varied
from nearly 60 days in digestive gland to only 15 days in gonad.
Since the 1966 ban on alkylmercury seed dressing in Sweden the mercury
content of feathers from selected raptorial and seed-eating birds has de-
creased. Feathers from museum-preserved birds collected prior to the use
of mercurial seed dressings also contained low mercury concentrations
(Westermark ejt al_. 1975). Olsson (1976) performed a similar before-and-
after study below a Swedish paper mill. Four years after mercury dis-
charges were discontinued, northern pike contained significantly 'less
mercury; males contained higher mercury levels than females and size was
more closely correlated with mercury level than age. For fish of the same
length, individuals with a low condition factor contained more mercury than
those with high condition factors, indicating that mercury concentration
increases in the fish during periods of starvation. Norwegian workers
(Steinnes et_ al_. 1976) found that fishes collected below the outfalls of
a pulp and paper mill five years after a ban on mercury contained con-
siderably less mercury than fishes collected prior to the ban; however,
the levels were still unacceptable for human consumption. Livers from
these fish contained unusually high mercury levels with some livers exceed-
ing 200 yg Hg g'1. The ratios of mercury in liver to that in muscle for
these fish were much higher than ratios reported bv earlier workers
(Jernelov and Lann 1971). Caines and Holden (1976) examined a case of
mercury pollution in a Scottish river. Mercury entered the river from an
industry prophylactically treating seed potatoes with methoxyethylmercuric
chloride. Some brown trout and grayling (Thymallus thymallus) attained
mercury levels in muscle approaching 20 and 12 yg g"1 respectively. How-
ever, mercury levels in fish returned nearly to background within one year
after the discharge was stopped. This unusually fast recovery was
43
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attributable to the finding that most of the mercury in these fish was
present in forms other than methylmercury.
Looking at dam lakes in Bohemia Hejtmanek ejt al_. (1975) found one lake
where 40 percent of the fish analyzed contained mercury levels surpassing
0.5 yg Hg g-1. Northern pike generally contained higher mercury levels than
other species from a given lake. In a Bavarian study Knb'ppler and Dorn
(1976) surveyed the mercury content of fishes from various waters including
fish culture ponds and the rivers Danube, Naab and Altmiihl. Pond fishes had
very low mercury levels (0.01 to 0.22 yg g"1) and most fish from the Naab
and Altmuhl contained less than 0.5 yg g"3-. Danube River fishes were much
higher in mercury with some fish containing nearly 2.5 yg Hg g'1. However,
Gergely ejt aj_. (1977) found that fish from the Hungarian portion of the
Danube averaged only 0.59 yg Hg g"1 and fish from various other Hungarian
lakes averaged less than 0.5.
Jeyachandran and Raj (1975) analyzed several fish from a Tamil Nadu,
India, reservoir for mercury and found none exceeding 0.50 yg Hg g"1. In
Japan Matsunaga (1975) demonstrated that crucian carp (Carassius carassius)
concentrated mercury nearly 25,000 times the concentration present in river
water. Yamanaka and Ueda (1975) reported the unusual finding that high
levels of ethylmercury were present in fishes and sediments in the Jinzu
River, Japan, below the outfall Vf a- pharmaceutical company synthesizing
an antiseptic containing an ethylmercury derivative. Upon news of this
occurrence, the Japanese government dredged the river to eliminate the
contamination. Fish were monitored for mercury content following dredging
and it was found that four years were required for fish to return to normal
mercury concentrations. The half-time of ethylmercury in these fishes was
greater than one year.
The distribution and concentrations of mercury in marine organisms is
important because marine fishes and shellfishes are frequent human dietary
constituents. Arima and Umemoto (1976) found an uneven distribution of
mercury in muscle tissue from bigeye tuna (Thunnus obesus], bluefin tuna
(T. thynnus) and swordfish (xiphias gladius). This finding was attributed
to the fact that mercury has a higher affinity for myofibrillar protein and
sarcoplasmic protein than for non-protein nitrogenous compounds or insoluble
muscle residue. Mercury had the highest affinity for myofibrin.
German workers (Kruger et al_. 1975) collected fishes from north
Atlantic waters utilized by the German commercial fleet and analyzed edible
portions for mercury. Fish from most areas including Iceland, Newfoundland,
and the Faeroes did not exceed the 1.0 yg Hg g"1 permitted by the Federal
Republic of Germany. However, fish from the Elbe estuary contained extremely
high mercury levels. In another,survey of German fishing waters, older ling
(Molva molva) and red-fish (Sebastes marinus) were found to exceed 1 yg Hg
g"1 (Jacobs 1977). Bluefin tuna averaged 0.40 yg Hg g'1, ray (Hypotremata
sp.) averaged 0.77 and various sharks averaged 1.83. Between 70 and 98 per-
cent of the mercury was present as methylmercury. The mercury levels in
market fishes from the port of Genoa, Italy, were surveyed by Cugurra and
Maura (1976). Most fish species contained mercury levels below the FDA
guideline level but tuna (Thunnus thynnus, Oblata melama-a and Umbrina
44
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cirrhosa) exceeded the guideline. New Zealand snapper (Chrysophrys auratus]
were analyzed for mercury due to their commercial importance in the area
(Robertson et al_. 1975). Although fish from some bays averaged up to 0.72
yg Hg g-1 and extremely large individuals (50+ cm) averaged 1.00 vg Hg g'1,
the overall average marketable fish contained only 0.25 yg Hg g"1.
Nuorteva and Ha'sanen (1975) looked at the relationship between mercury
accumulation and size in fourhorn sculpin (Myoxooephalus quadricarnis L.)
collected from two areas of the Baltic and compared the mercury levels found
in this species to the mercury concentrations present in other species from
the same area. The relationship between mercury content and weight was
linear for fish from both areas; however, sculpins contained more mercury
than another bottom fish, the flounder (Platiohthys flesus). The higher
mercury content of sculpins was attributed to their having a more mercury-
rich diet than flounder.
Reimold and Shealy (1976) analyzed young-of-the-year finfish from bays
along the Georgia and South Carolina coasts for mercury during various
times of the year. Most individuals contained mercury concentrations well
below the FDA guideline. However, the spring 1973 samples of silver perch
(Bairdiella chrysura) from the South Santee River and Port Royal Sound, and
Atlantic croaker (Micropogon undulatus] from Winyah Bay contained mercury
levels in excess of 0.5 yg Hg g"1. The same species contained much lower
mercury levels the preceding and following falls; no explanation was ad-
vanced. Similarly, Greig ejt aj_. (1977) measured mercury concentrations in
organs and muscles from three fish species collected off the northeast coast
of the United States. Cusk (Brosme brosme) had higher concentrations of
mercury in muscle and liver than in gill or kidney but a blackbellied red-
fish (Heliaolenus dactylopterus) had similar mercury levels in all tissues.
Muscle tissue from spiny dogfish (Squalus acanfhias) had higher mercury
levels than organs, averaging 0.35 yg Hg g'1.
In the same species collected off the Oregon coast Childs and Gaffke
(1973) found an average level of 0.60 yg Hg g-*. Hall et a]_. (1977) mea-
sured mercury levels in spiny dogfish collected from inland marine waters
of the state of Washington. The mean mercury content of fish from all
sampling stations exceeded 0.9 yg Hg g'1; mercury tissue level was directly
related to fish weight, and males contained more mercury than females for
a given weight. Because females of this species are known to grow faster
than males, this latter finding was attributed to growth dilution. This
evidence suggests that more mercury is present in water off the Oregon-
Washington coast than in the North Atlantic and that inland waters are
more severely contaminated. Hall et;al_. (1976a) collected halibut
(Hippoglossus stenolepis] from various locations along the Pacific coast
of North America and measured the mercury content of muscle tissue.
Mercury was evenly distributed in the entire edible portion. The average
concentrations for fish of similar size steadily increased moving south
from the Bering Sea down to the Oregon-Washington coast. The authors
speculated that this trend may reflect the degrees of mercury contamination
for the various latitudes of the Pacific Ocean. The same north to south
trend was noted in a similar study of Pacific sablefish, Anoplopoma f-imbria
(Hall et al_. 1976b).
45
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Eganhouse and Young (1976) measured the mercury content of mussel
(Mytilus califomianus} from various locations along the California coast
between San Diego and just north of Santa Barbara. Specimens collected
near harbors and municipal and industrial outfalls generally contained
more mercury. Flegal (1977) reported a similar finding for seston from
San Francisco Bay; phytoplankton and organic detritus contained more
mercury than zooplankton. The same trend was noted for most fish and shell-
fish collected from the Georges River—Botany Bay estuary, an area known
to receive large amounts of industrial and domestic effluents from Sydney,
Australia (Wi 11 i ams ejt a]_, 1976). Sidney rock oysters (Crassostrea
cormercialis) from Botany Bay were significantly higher in mercury than
oysters from areas receiving less pollution; but other organisms analyzed,
including blacklip abalone (HalioHs ruber), blackfish (Girella triauspidata)
and bream (Acanthopagrus sp.) had about the same mercury content regardless
of collection location.
Shultz e_t a_l_. (1976) reported on the mercury content of blue marlin
(Mdkaira nigrioans) caught off the coast of Hawaii. Unlike most fish,
marlin contained more inorganic mercury than methylmercury. Muscle averaged
2.42 vg Hg g"1 of which only 0.36 yg g"1 was organic. The relationship was
particularly striking in liver where the ratio of inorganic mercury to
^methylmercury was 35 to 1. Perhaps marlin are unusually efficient at de-
Wthylating mercury. The authors suggested that the frequent volcanic
activity in the islands area may contribute mercury to surrounding waters.
Hawaiian inshore organisms were found to contain relatively low mercury
levels (Kl emmer crt a_]_. 1976); all individuals including a variety of sessile
and mobile invertebrates and benthic and pelagic fishes averaged less than
0.33 yg Hg g"1 and most species averaged less than 0.15.
In summary, methylmercury is the form of mercury present in most fish
tissue and is the most readily accumulated and retained form of mercury in
biological systems. Most mercury occurring in water, particularly problem
amounts, can be traced to man-caused sources; however, fish mercury levels
exceeding the FDA guideline have in some instances been attributed to
natural sources. Upon entering water, virtually any mercurial compound may
be microbially converted to methylmercury. Conditions reported to enhance
the methylation process include large amounts of available mercury, large
numbers of bacteria, absence of strong complexing agents such as sulfide,
neutral pHs high temperature, and a moderately aerobic environment. De-
methyl ati on processes also occur but apparently only when methylmercury
levels become excessive. Bacteria not only act as methylators of mercury
but also preferentially accumulate large amounts of mercury; however,
sediment and water are probably the two most important mercury sinks.
Conditions reducing the mercury content of overlying waters, such as the
accumulation of mercury by aquatic organisms, result in the mobilization
of mercury from sediment.
Methylmercury is readily accumulated by fishes both from their food
and through the water. Although conflicting evidence exists as to the rela-
tive importance of these two sources of mercury to fishes, most reports
suggest that both sources can be significant. Upon entering a fish,
methylmercury is very difficult to eliminate; most studies imply that the
46
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biological half-time of methylmercury in fishes is between one and three
years. Hemoglobin has been shown to be the major transporting agent for
methylmercury in the body, not only transporting methylmercury to the various
tissues and organs but also receiving methylmercury from proteins during
elimination. In muscle protein mercury is not uniformly distributed because
methylmercury has a higher affinity for myofibrin and sarcoplasmic protein
than for other muscle fractions.
Fishes are able to tolerate very high tissue burdens of mercury. Fat-
head minnows exposed to 0.078 yg Hg x,"1 as methylmercury and brook trout
exposed to 0.03 yg Hg a~l as methylmercury attained mercury levels in edible
portions exceeding the FDA action level (0.5 yg Hg g"1) without suffering
adverse effects. In fact, rainbow trout have accumulated up to 30 yg Hg g"1
without noticeable effects. Thus, regulations regarding mercury in water
must primarily be concerned with protecting human consumers of fish.
Differences in the mercury content reported between and among species of
fish from a given environment are reportedly due to variations in age,
surface area, metabolic rate, habitat, and activity of the fish.
Methods have been suggested for decontaminating mercury-laden environ-
ments, but all are time-consuming and costly. Although in most instances
economic factors preclude effective removal of mercury from most lakes and
streams, several studies have shown marked improvements in aquatic environ-
ments once mercury discharges were ceased.
47
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SECTION XVI
•MOLYBDENUM
Molybdenum is used as a lubricant, an alloy in steel and as a catalyst
in petroleum processing. In addition, molybdic acid is used by the ceramic
industry (NAS 1973). Although molybdenum is a trace nutrient for plants,
livestock consuming plants from areas containing high levels of molybdenum
in soil have developed toxic symptoms (Chappell 1975). Toxicity results
from a copper deficiency resulting from molybdenum's replacing copper.
Molybdenum may enter the aquatic environment through leaching processes
near molybdenum mines, burning of fossil fuels, or natural weathering
processes. Molybdenum is known to be an important micronutrient for algae;
however, very little information is available on the accumulation of molyb-
denum by fishes.
Ward (1973) measured the molybdenum content of tissues from rainbow
trout (Salmo gairdneri] and kokanee salmon (Oncovhynchus nerkz] collected
from waters containing 0, 6, and 300 yg Mo a"1. Although some tissues such
as bone, kidney, and brain increased in molybdenum content as the molybdenum
content of the water increased, other tissues including skin and muscle
contained similar molybdenum concentrations regardless of the molybdenum
concentration in water. Rainbow trout contained consistently more molyb-
denum than kokanee salmon collected from the same water; however, the
relative ages of these two species were not known. In lake trout
(Salvelinus namayaush] from Lake Cayuga, New York, molybdenum content
actually decreased with fish age (long et_ aJL 1974). Goettl and Davies
(1977) exposed rainbow trout to various molybdenum concentrations in water
for periods of up to 492 days and measured molybdenum accumulations by
liver. Trout exposed to the highest molybdenum level (18.7 mg Mo £-1)
accumulated significantly more molybdenum than controls', but lower expo-
sures resulted in insignificant molybdenum uptake.
Molybdenum does not tend to accumulate in the edible portions of fishes
and has a relatively low toxicity to humans. In addition, trace amounts of
molybdenum are important for the growth.of phytoplankton. Molybdenum in
aquatic environments is, therefore, of little danger to humans. Because
molybdenum replaces copper, it might be instructive to explore molybdenum's
influence on the toxicity of copper to fishes.
48
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SECTION XVII
NICKEL
Nickel is a common component of some metal plating industry wastes, is
a constituent of metal alloys (Pickering 1974), and is present in the emis-
sions from coal combustion. Some organic nickel derivatives, particularly
nickel carbonyl, are highly toxic to humans. However, orally ingested
nickel has a very low toxicity to man. Although metallic nickel is in-
soluble in water, some nickel salts are quite soluble (Kopp and Kroner
1970). Because of nickel's low toxicity to humans, almost no information
is available on the accumulation of nickel by aquatic animals.
Friedrich and Filice (1976) studied the accumulation of nickel by
mussel (Mytilus edulis) kept in artificially prepared seawater under static
conditions. No significant accumulation was noted after four weeks' expo-
sure to 0.03 mg Ni XT1, but significant uptake was noted at all concentra'-
tions exceeding 0.056 mg Ni &"*; rates of nickel elimination were not
measured. In a study of the accumulation of iron, zinc, lead, copper and
nickel by algae collected near a zinc smelting plant it was found that
nickel exhibited the lowest concentration factor for all the metals tested
(Trollope and Evans 1976). Panel on Nickel (1975) have summarized available
information on the nickel concentrations found in various marine and fresh-
water fishes or shellfishes. Most foods including clams, scallops, shrimp,
lobsters, crabs, marine fishes and freshwater fishes contained nickel
levels below 0.75 yg Ni g-1; however, fresh oysters and Pacific salmon
contained higher nickel levels, averaging 1.50 and 1.70 yg Ni g"1 respec-
tively. Pringle et al_. (1968) found from 0.12 to 1.74 yg Ni g'1 in
oysters (Crassostrea virginica) collected along the eastern coast of the
United States. Wright (1976) observed nickel concentrations exceeding 7.0
yg Ni g"1 in muscle from marine fishes collected from the northeast coast
of England, and Romeril and Davis (1976) reported that European eels
(Anguilla anguilla) maintained in Trent River water averaged (dry basis) 21
yg Ni g"1 in muscle and 16 in liver.
Apparently, elemental nickel is not a human health concern in the
aquatic environment because nickel is not accumulated in significant
amounts by aquatic animals, and since orally ingested nickel has a very
low toxicity to humans. Concern over nickel in water should focus on its
effects on aquatic life.
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SECTION XVIII
PLUTONIUM
Nuclear testing programs carried out among the major world powers
have resulted in the release of a considerable amount of radioplutonium to
the environment (Schell and Matters 1975). Plutonium from this source
enters water primarily through atmospheric fallout. In addition, plutonium
may enter water in the wastes from nuclear powered electrical facilities
and from nuclear fuel reprocessing plants. Over the pH range of most
natural waters, plutonium is present either in the trivalent or hexavalent
form.
Studying plutonium in organisms collected off the coast of France in
an area receiving effluents from a nuclear fuel reprocessing plant, Guary
e_t aj_. (1976) found that crab (Cancer pagurus) accumulated highest plutonium
levels in gill and exoskeleton, whereas plaice (Pleuronectes platessa)
attained highest concentrations in gut. This result suggests that food is
an important source of plutonium to plaice. However, in a more comprehen-
sive study of marine littoral organisms from the same area, Guary and
Fraizier (1977a) observed a decrease in plutonium concentration factor
with increasing trophic level. Plutonium was preferentially accumulated
by animals with calcareous exostructures such as mussels and lobsters;
calcareous plants also attained high plutonium levels. Although food was
definitely a source of plutonium to animals at higher trophic levels, the
increment of plutonium provided by food was not great enough to cause a
positive correlation between trophic level and tissue plutonium accumula-
tion. Miettinen e_t al_. (1975) noted a similar lack of correlation between
trophic level and plutonium content in marine organisms collected from the
Baltic Sea near Finland.
A spatial study of plutonium in various molluscs collected within the
plume of a nuclear fuel reprocessing plant revealed that only animals within
50 km or less of the reprocessing plant contained plutonium concentrations
greater than could be attributable to fallout (Guary and Fraizier 1977b).
Unlike molluscs from most areas, molluscs collected near the reprocessing
plant contained higher plutonium concentrations in soft tissues than in
shell. This observation was attributed to possible differences in the
isotopic composition of plutonium near the plant.
Noshkin (1972) reviewed various surveys of the plutonium levels found
in marine organisms and pointed out that bottom feeding organisms always
accumulated more plutonium than other organisms from the same environment.
Edible muscle from marine fishes and shellfishes accumulated very little
50
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Plutonium, usually having a concentration factor of less than ten; but gut
and bony structures accumulated much higher levels. Similarly, Schell and
Matters (1975) reported low plutonium concentrations in fishes collected
near former nuclear testing sites. Ward (1966) reported that lobster
(Homavus vulgaris) exposed to 239Pu in seawater for over 200 days also
preferentially accumulated plutonium in hard parts. Almost 90 percent of
the 239Pu was in the shell; flesh contained only 1.2 percent of the 239Pu
in the body. The concentration factor for flesh was only three (dry basis).
Fowler ejt al. (1975) also noted Plutonium's high affinity for bony struc-
tures, narneTy the shells of common Mediterranean mussel (Mytilue
galloprovinciaHs) and the exoskeletons of benthic shrimp (Lysmata
seticaudata). The biological half-time of plutonium in the mussels was
near two years but in shrimp the half-time was only 1.5 months due to the
loss of plutonium during molting.
Chelation of metals with certain ligands is known to increase the solu-
bility of some metals in water but little is known about the biological
availability of these ligand-metal complexes. Eyman and Trabalka (1977)
examined the intragastric availability of two plutonium complexes (Pu-fulvate
and Pu-citrate) to channel catfish (ictalurus punctatus) and compared the
retention of these complexes to that of plutonium hydroxide. Each of
several catfish was exposed via a single injection to one of the isotopi-
cally labeled plutonium compounds. Pu-citrate was found to be retained
much more readily than Pu-hydroxide presumably due to its net negative
charge but Pu-fulvate was only modestly retained. This latter finding was
believed to result from the stability of this complex in the digestive
tract and its high molecular weight.
Plutonium is accumulated by aquatic organisms from both food and water,
and calcareous structures such as bone or shell attain the highest levels.
Chelation of the metal influences its biological availability but the extent
and direction of this influence depends on the particular ligand-metal
complex. Edible muscle tissue from fish accumulates very little of the
isotope, but some reports indicate that the form of isotopic plutonium
present in nuclear fuel reprocessing plant effluents is readily accumulated
in the soft tissues of some marine molluscs. Because the isotope is ex-
tremely hazardous, the consumption of marine molluscs and aquatic species
which are usually eaten in their entirety (e.g., sardines and herring)
should be restricted if contamination is suspected.
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SECTION XIX
RUTHENIUM '
Ruthenium is rare in nature, occurring as the metal and in arsenide,
sulfide, and other ores. Ruthenium is also a fission product of uranium
and is used as a platinum and palladium alloy, as a catalyst, and as a dye
in ceramics (Weast 1975; McKee and Wolf 1963).. Ruthenium-106 is common in
the effluents from nuclear fuel reprocessing plants, therefore its presence
in the aquatic environment has received some attention.
Ishikawa et^al_. (1976) measured 106Ru uptake and elimination by the
marine clam (Meretrix meret'rix lusoria) as an initial step in determining
the influences of ruthenium from a Japanese nuclear fuel reprocessing plant
on the marine environment. Clams attained highest ruthenium levels in mid
gut gland followed in decreasing order by gil^l, visceral mass, mantle,
shell and foot. The" concentration, factor for gill'Was 10. Prepared
ruthenium was present either as purified 106Ru«Clx or 106RuNO-Clx, and pur-
chased ruthenium was present as crude 106Ru«Clx or 106RuNO'(N03)x. Pre-
pared ruthenium was accumulated slightly more readily than purchased forms,
and RuNO-Clx was eliminated faster than Ru«Clx. Ruthenium elimination was
characterized by two phases, the first having a biological half-time of
39.3 to 48.7 days and the slower second phase having a half-time of 121.2
to 166.7 days. The fast phase represented elimination from soft parts,
whereas the slow phase was due to elimination from shell.
Jones (I960) studied ruthenium uptake by marine organisms and sedi-
ments and determined the influences of the source of the ruthenium and the
presence of iron on uptake. Marine algae absorbed 106Ru in amounts propor-
tional to their surface areas, but the extra-cellular composition of the
algae was also a determining factor. Mussel (Mytilus edulis] accumulated
highest amounts of 106Ru in shell whereas plaice (Pleuronectes platessa)
contained highest 106Ru levels in gill, gut and skin with very little in
muscle. Nitrosyl 106Ru was complexed by iron, making it less available to
biota. Organisms accumulated commercial ruthenium more readily than
ruthenium present in nuclear reactor effluents.
Berg and Ginsberg (1976) collected and analyzed ruthenium-contaminated
crayfish (Orconectes obscurus> 0. rusticus rusticus, Cambarus robustus and
C. bartoni bartoni) from a New York creek and performed ruthenium uptake
studies with two species of crayfish (c< robustus and C. rusticus) in the
laboratory. The laboratory experiments showed that crayfish species and
sex, and whether the tracer was present as a chloride or nitrate derivative,.
had little influence on uptake, but physical form of the additive, route of
52
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uptake, and mode of administration all influenced accumulation. Suspended
particulates decreased uptake, ruthenium present in food increased the
visceral content of ruthenium, and ruthenium was concentrated to a greater
degree by conditioned individuals than by new crayfish added to the same
medium. Concentration factor ranged from three to nine depending on the
medium. Most ruthenium in the crayfish was associated with exoskeleton.
whereas gill and muscle contained very little ruthenium. Viscera contained
substantial amounts of ruthenium when ruthenium was present in the diet,
but accumulated negligible amounts when water was the only source of the
isotope. Crayfish collected from Buttermilk Creek, New York, had highest
ruthenium levels in digestive gland followed by gill, carcass, abdominal
muscle and body fluids. Fish from the same creek contained considerably
less ruthenium than crayfish. Crayfish were suggested as indicator organ-
isms for detecting ruthenium contamination. Harrison (1973) also found
that fishes accumulated very little ruthenium (as 103Ru); however, crayfish
(Astacus sp.) in freshwater and crabs (Cancer productus] in saltwater
exhibited concentration factors ranging from three to seven in visceral
organs.
The chemical form of the .ruthenium and the chemical characteristics of
the water influence the accumulative properties of the isotope. Although
the concentration factors reported for aquatic organisms are quite low, the
biological half-time of ruthenium is high. Shellfishes appear to concen-
trate ruthenium more readily than fishes, and ruthenium in fishes does not
lodge in edible muscle tissue. Instead, the internal organs, gills and
skin of fishes preferentially accumulate ruthenium. In crayfish, the mode
of exposure influences the distribution in the body. Although ruthenium is
not readily accumulated by aquatic organisms, the occurrence of the radio-
isotope in seafoods may present a potential hazard to humans.
53
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SECTION XX
SELENIUM
Selenium is commonly used in industry and agriculture and occurs in
relatively high concentrations in fossil fuels and some natural sediments.
Selenium, therefore, reaches natural waters via both fallout and runoff.
Plants growing in geographic regions possessing highly seleniferous soils
usually contain high concentrations of selenium. The consumption of these
plants by grazing animals has resulted in alkali disease or selenium poison-
ing (Berry et_ aJL 1974). Symptoms include lesions of internal organs,
characterized by congestion and hemorrhages. Industrial accidents have
resulted in selenium poisonings in humans, but poisonings are more common
in other animals. Beal (1974) described the symptoms of human selenium
poisoning in detail; poisoning is characterized by anemia, nervousness,
hypertension, depression, gastrointestinal disturbances and garlic odor
of the breath and perspiration.
The toxic action of selenium reportedly results from its inhibition
of sulfur enzymes (Berry ejt aj_. 1974). However, selenium in the diet is
known to exert a protective influence against mercury poisoning. Japanese
quail and rats fed a tuna diet containing selenium and methylmercury were
less susceptible to methylmercury poisoning than individuals fed a corn
soya diet containing only methylmercury (Ganther and Sunde 1974). Sell
and Horani (1976) reported a similar finding for chicks and Japanese quail;
in their experiments dietary selenium reduced methylmercury accumulations
by 50 percent. .Koeman et_ a_]_. (1973) have shown that mercury and selenium
are present in the livers of marine mammals in a 1:1 molar ratio whereas
marine fishes usually contain upwards of 40 times more selenium than
mercury. This result suggests that selenium and mercury may occur together
in marine mammals, perhaps resulting in some degree of protection against
mercury.
Kim ejt aj_. (1977) found that creek chubs (Semotilus atromaculatus)
immersed in water containing 3.0 mg Se JT1 for 48 hours were less suscep-
tible to mercuric chloride in water than untreated individuals. Interest-
ingly, at mercury concentrations below 0.07 mg Hg &-1 selenium treatment
increased mercury accumulation; but at mercury levels above 0.10 mg Hg
a"1 selenium inhibited mercury accumulation. No speculations were offered
as to the mechanism of this action.
Sandholm et al_. (1973) studied selenium uptake in a laboratory food
chain consisting of water, phytoplankton, zooplankton and fish; both
selenite and selenomethionine were used. In these experiments food was
54
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determined to be the most important source of selenium to fish because very
little selenium was accumulated via the water route.
In a saltwater study, Fowler and Benayoun (1976a) measured selenium
uptake in a marine shrimp (Lysmata setioaudata] exposed to 75Se in food and
water and in a mussel (MytiluB galloprovinciaHs) exposed to 75Se in water.
Shrimp exoskeleton contained 60 to 90 percent of the 75Se accumulated when
exposure was through the water, but viscera had the highest activity when
selenium was accumulated, via food. Exoskeleton contained 20 to 45 percent
of the selenium accumulated from food. Only 10 percent of the selenium
present in exoskeleton was lost during molting. The selenium distribution
in shrimp accumulating selenium from food was similar to the distribution
of selenium found in shrimp in nature. Mussels accumulated the highest
concentrations of selenium in viscera. Selenium concentrations continued
to increase in all tissues analyzed (gill, muscle, shell, viscera, mantle
and whole body) after 63 days' exposure. The greatest percentage of total
selenium in the animal (40 to 60 percent) occurred in the shell. Fowler
and Benayoun (1976b) reached a similar conclusion with euphausiids
(Meganyatiphanes norvegica). Dietary selenium was retained at an efficiency
of 66 percent. Viscera attained the highest concentration of selenium and
molted exoskeletons contained from 3 to 8 percent of the selenium which had
been accumulated. The biological half-time of selenium was 37 days and
whole body concentration factors were estimated at 1500 to 7500 for this
species.
Beal (1974) measured the selenium content of fishes from various fresh-
waters in central Canada and found an average whole body selenium content
of 0.33 yg g"1 with values ranging from 0.04 to 2.00. In a similar survey
of fishes from New York State waters Pakkala et al_. (1972) observed compar-
able values. Barnhart (1958) found high level? of selenium in fish from
an artificial Colorado lake located in a highly seleniferous region. The
inability of stocked fish to survive for extended periods of time in this
impoundment was attributed to fish accumulating excessive selenium through
their food chain. Analyses of aquatic organisms from various fresh and
marine waters near Finland revealed that marine fishes usually contained
1 to 2 yg Se g'1 whereas freshwater fishes ranged from 2 to 3 (Sandholm ejt
al. 1973). Marine plankton contained selenium levels similar to those in
fish; however, aquatic flowering plants had extremely low concentrations of
selenium.
What little information is available suggests that dietary selenium is
the most important source of selenium to many marine and freshwater organ-
isms; however, this has not been confirmed. Fishes do not appear to con-
centrate selenium at levels which would be dangerous to human health; in
fact, in some instances the accumulation of selenium by fishes may be
beneficial to both fishes and to human consumers of fishes due to the
protective action selenium provides against mercury. However, because of
selenium's high toxicity, the relationship between selenium toxicity to
aquatic organisms and selenium accumulation requires further attention.
55
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SECTION XXI
SILVER
Silver is one of the most toxic metals to aquatic life, ranking ahead
of mercury on a relative acute toxicity basis (Doudoroff and Katz 1953).
Silver is used in photography, silverware, metal alloys, electroplating,
ink, food and beverage, and porcelain (Weast 1975, McKee and Wolf 1963).
In addition, silver iodide is an effective nucleating agent in weather
modification (Cooper and Jolly 1970). Although natural weathering pro-
cesses contribute some silver to natural waters, most silver salts are
insoluble in water (McKee and Wolf 1963). Effluents from the photoprocess-
ing industry contribute silver to natural waterways (Terhaar ejt'aJL 1977):.
Over-exposure to silver by humans- results in graying of the skin, eyes, and
mucous membranes (argyrosis). However, because of the low solubility of
most silver compounds, very little is accumulated by mammals.
••*,••«..
Cearley (1971) found that juvenile largemouth bass (Miaropterus
salmoides] and bluegill (lepomis macroehirus) exposed to 0.01 or 0.001 mg
Ag jr1 for six months continued to accumulate silver for two months then
leveled off. Internal organs contained more silver than muscle tissue.
Similarly, Coleman and Cearley;(1974) exposed largemouth bass and bluegill
to several silver concentrations in water (from 0.3 to 70 yg Ag £~1) for
up to six months and measured silver accumulation in various tissues from
bass and in whole bluegill. Silver uptake by both species was rapid during
the first two months but then slowed considerably. Gill and internal
organs from bass (including liver, kidney, spleen and digestive system)
reached much higher silver levels than did the remainder of the fish,
demonstrating that muscle tissue accumulates little silver. Concentration
factor for the gills of bass was near 200, and whole bluegill concentrated
silver in gill up to 120-fold. These findings are in agreement with those
of Goettl e_t al_. (1974) who measured silver concentrations in tissues of
cutthroat trout (Salmo olarki] collected from an alpine lake located in a
region underlying an atmospheric zone undergoing extensive cloud seeding
with silver iodide. Silver concentrations (in yg Ag g~! dry tissue)
ranged from: 1.92-4.40, bone;-0.09-0.99, muscle; 1.08-2.21, liver; 0.32-
0.92, gonads; 0.00-0.79, skin; Q-.28-0.50, gut; and 0.18-0.50, kidney.
Hibiya and Ogura (1961) measured the distribution of 110Ag, five to seven
days after a single dose of the isotope was injected into the air bladders
of goldfish (Carass-ius awcatus]. During this experiment liver and air
bladder attained higher silver levels than other organs.
Terhaar et_ ial_. (1977) have shown that an alga (Soenedesmus sp.),
Daphnia (Daphnia magna], freshwater mussels (Ligtmia sp. and Margaritifera
56
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sp.) and fathead minnows (Pimephales promelas) are all capable of accumulat-
ing silver from water; but the food chain was not an important route of
silver accumulation for animals at the higher trophic levels. Thurberg et_
al. (1974) measured silver levels in marine bivalves following 96 hours'
exposure to either 0.5 or 1.0 mg Ag &"1. Gills contained higher silver
levels than the rest of the body and individuals exposed to the higher
concentration accumulated slightly more silver than those exposed to 0.5
mg Ag x,"1, but the difference was not proportional to exposure level.
Elimination rates were not measured.
In surveys of the metals content of fish from both marine (Greig et_
al_. 1976; McDermott ejt aU 1976) and freshwater (Lucas et al_. 1970; long
e_t al_. 1974) environments, silver was always present at~Tow concentrations,
usually less than 0.1 pg Ag g"1. Red abalone (Haliotis rufesaens) from
the California coast contained 13 to 129 yg Ag g"1 in gill, mantle or diges-
tive gland (dry basis) but only 1.1 to 44 ug Ag g"1 in foot (Anderlini 1974),
The silver concentration in foot averaged only one-tenth that found in other
organs. An apparent inverse relationship was noted between the silver and
copper content of abalone.
Silver is not present in aquatic animals at very high concentrations
because most of its compounds are virtually insoluble in water and silver
has a very short biological half-time; moreover, ingested silver has a very
low toxicity to humans and does not accumulate significantly in the edible
portions of fish. This combination of characteristics decreases the hazards
associated with consuming silver-exposed aquatic organisms; but because of
silver's high toxicity to aquatic life, threshold levels of silver in key
organs should be determined.
57
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SECTION XXII
STRONTIUM
Radioactive strontium may enter the environment as a result of nu-
clear detonation or in effluents containing nuclear wastes. Strontium
fallout easily enters ground and surface waters since strontium is not
appreciably absorbed by soils (McKee and Wolf 1963). Strontium is chemi-
cally similar to calcium and is therefore deposited in bony tissues.
Because of this bone-seeking tendency, radiostrontium is extremely danger-
ous; however, non-radioactive strontium is almost nontoxic to man.
Brungs (1967) observed that animals with exoskeletons (crayfish) or
shells (clams, snails) were capable of accumulating much higher 85Sr levels
than animals containing higher percentages of soft tissues. However, cray-
fish (Ccmbarus longulus longerostris] have been shown to lose most of their
accumulated 85Sr during molting (Schurr and Stamper 1962). Although stron-
tium was readily accumulated by crayfish, the biological half-time was only
about two days. In a lake receiving radioactive wastes strontium concentra-
tion factors in the hard parts of fish reportedly exceeded 30,000 (Krumholz
1956). Increasing calcium concentrations in water decreased strontium up-
take by aquatic organisms due to the similarity of the two elements
(Williams and Pickering 1961; Preston et a]_. 1967). Feldt (1963) demon-
strated this trend by showing that strontium levels in fishes from various
seas and lakes were inversely related to salinity in saltwater and to hard-
ness in freshwater.
Schiffman (1961a) measured strontium flux in perfused gills from rain-
bow trout (Salmo gairdneri], Trout were able to excrete strontium even
against a concentration gradient, suggesting that the ability of trout to
concentrate strontium must result from a binding mechanism reducing the
diffusibility of ionic strontium. Dialysis studies with strontium in blood
confirmed that nearly 50 percent of the strontium was present in a nondialyz-
able form. In another study Schiffman (1961b) injected a single dose of
85Sr into the dorsal aorta of a urinary bladder cannulated rainbow trout.
After 24 hours 6 to 7 percent of the 85Sr was in the urine, 3 to 4 percent
in the gut and 50 to 75 percent remained in the fish. These results suggest
that 15 to 40 percent was excreted via the gills or skin.
Nakatani and Foster (1963) fed varying levels of 90Sr-90Y to rainbow
trout for up to 25 weeks. About 25 percent of the oral dose administered
was retained by the trout, and bony tissues contained the highest concentra-
tions. Ophel and Judd (1967) examined some of the factors governing radio-
strontium accumulation from food in the goldfish (Carassius awratus}. Fish
58
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were force-fed the radioactive diet followed by a voluntary feeding of a
control diet. Calcium and magnesium in the diet reduced the retention of
90Sr from the diet. The concentration factor for dietary 90Sr was 250-500.
Increasing the time interval between the isotope force-feeding and the
voluntary control feeding increased the efficiency of dietary 90Sr uptake.
Tripling the specific activity of the food resulted in only a slight de-
crease in retention efficiency of the isotope. Similarly, Schiffman (1959)
measured the retention of ingested 90Sr-90Y by rainbow trout when the
isotope was present in a natural diet or in a gelatin capsule. Twenty-one
percent of the encapsulated strontium was retained by the trout but only
seven percent of the isotope present in the natural die.t was retained.
Strontium accumulated from food and water were additive. Based on the
retention of strontium from the natural diet, water was calculated to be
ten times more important than food as a source of strontium to fish in
nature.
Shealy and Carlson (1973) exposed various life stages of largemouth
bass, (Mioropterus salmoides} including embryo, prolarval, postlarval and
juvenile, to 85Sr in water and measured accumulation and retention of the
isotope. Strontium was retained longer as the bass became older, presumably
due to an age-related increase in percentage of bony structures. Rosenthal
(1963) measured strontium uptake and turnover in the guppy (Lebistes). Up-
take was linear over the 15-day experiment. Viscera lost strontium rapidly
with a biological half-time of only eight days but the half-time for the
rest of the body including muscle tissue was over two years. Guppies showed
only a slight preference for calcium over strontium. Martin and Goldberg
(1962) followed the uptake and elimination of 90Sr in various organs and
tissues from Pacific mackerel (Pneumatophorus diego) following a single oral
inoculation of the isotope. Ninety-five percent of the dose was excreted
during the first 24 hours following inoculation, but the remaining five per-
cent remained in the fish for the duration of the 235-day experiment. The
retained 90Sr (80 percent) was located in bony tissue, where the concentra-
tion remained constant throughout the experiment. Strontium increased
rapidly in gill followed by a steady decrease, suggesting that this organ
is important in strontium excretion. Edible muscle tissue retained very
little of the isotope.
Strontium is readily accumulated and retained by fish from either their
food or water. Calcium competes with strontium in the uptake process, thus
organisms accumulate less strontium in calcium-rich waters. Upon entering
fish, strontium is eliminated primarily through the gills. Strontium is
chemically similar to calcium and is therefore bone-seeking; thus aquatic
organisms with high percentages of bone tend to accumulate high levels of
the metal. Bone-bound strontium is retained for long periods of time by
non-molting animals; however, non-radioactive strontium has a very low
toxicity both to aquatic animals and to man. Fishes such as sardines which
are consumed in their entirety represent the greatest risk to humans, and
soft waters contaminated by the radioisotope offer the optimum conditions
for isotopic bioaccumulation.
59
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SECTION XXIII
ZINC
Zinc has relatively low abundance in nature, but occurs widely in a
number of minerals. Zinc is extensively used in alloys, for galvanizing,
and for die castings; it is also used in the manufacture of paints, cos-
metics, pigments, electrical equipment, and other products (Weast 1975).
Zinc is an essential element for human and animal growth. Zinc is also an
important cofactor for certain enzymes (Lehninger 1970) and has a relatively
low toxicity to man. However, over-exposure by humans to zinc oxides or
chlorides has resulted in flu-like symptoms and pneumonia (Berry et al.
1974). Zinc enters water in numerous industrial effluents and through acid
mine drainage. In addition radioactive zinc is released during nuclear
explosions. Zinc sulfate and halides are soluble in water but the carbonate,
oxide and sulfides are insoluble (Weast 1975) .,,,Zinc toxidty to fishes
decreases with increasing water hardness (Mount 1966; PicfTering and Henderson"
1966; Sinley et_ aj_. 1974). In static bioassays zinc toxicity was reported
to decrease with increasing pH (Sprague 1964;'Cairns et_ a]_. 1972). However,
Mount (1966), using flow-through tests, observed that zinc was more toxic
with increasing pH; a possible explanation for this was that in static bio-
assays insoluble zinc settles out of solution, whereas in flow-through sys-
tems it remains in suspension.
Zinc has been extensively studied in the freshwater environment. Zinc-
65 was accumulated much more readily than 60Co, 137Cs or 85Sr by soft tissues
of carp, snails, tadpoles and clams during radioisotope experiments conducted
in ponds (Brungs 1967). During laboratory experiments brown bullhead
(lotalurus nebulosus) accumulated 55Zn rapidly for the first seven hours'
exposure followed by a reduced accumulation rate (Joyner 1961). Gill and
viscera reached the highest zinc concentrations of the tissues analyzed.
The esophagus was plugged on some fish to determine the fraction of zinc
accumulation attributable to swallowed water; this route of uptake was found
to be negligible. Zinc-exposed fish transferred to fresh water lost half of
their accumulated zinc after six days followed by a period of reduced zinc
elimination. Willis and Jones (1977) determined that zinc elimination in
juvenile mosquitofish (Gambusia affinis) was derived from three separate
zinc reservoirs having biological half-times of 2, 14 and 235 days; relative.
compartment sizes (as percent of total zinc present in the fish) were re- -
ported to be 9, 4, and 91, respectively. Thus, most of the zinc accumulated
is slowly eliminated. • •
Hodson (1975) studied the influence of temperature on zinc accumulation
by the gills of Atlantic salmon (Salmo salar] and related zinc uptake to '
60
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lethal response. Temperatures of 3, 11 and 19 C were tested, and fish were
exposed to about 14 mg Zn a~l. Zinc uptake increased as temperature in-
creased, presumably due to a temperature-related increase in metabolic
rate. Salmon killed by zinc at 19 C contained significantly more zinc than
individuals killed by zinc at lower temperatures. This finding corresponds
with the observations that the lethal threshold for zinc increases with
temperature and demonstrates that higher tissue residues are necessary to
kill salmon as temperature increases, suggesting that the site of toxic
action is more resistant at higher temperatures.
Goettl et_ aj_. (1972) measured zinc uptake in various tissues from
rainbow trout (Salmo gairdneri] exposed to zinc in water for up to 92
weeks. Eye accumulated the highest concentration of zinc followed by gill,
bone, intestine, liver, kidney and skin. Baseline zinc levels (dry weight
basis) for selected tissues from unexposed fish were (in yg g"1): eye 400,
skin 90, gill 200, opercular bone 195, stomach 1, liver 150, muscle 20,
kidney 125 and intestine 190. In another study Goettl e_t al_. (1974) found
that rainbow trout accumulated zinc in eye, gill arch and opercular bone in
proportion to zinc concentration in water after exposure to zinc levels
ranging from 71 to 260 yg Zn a~l for up to 77 weeks. However, for fish
exposed to any given exposure concentration, zinc in opercular bone decreased
in time. Slater (1961) found that fingerling brook trout (Salvelinus
fontinalis) and cutthroat trout (Salmo alarki] accumulated 65Zn more readily
than fingerling rainbow trout; gill filaments accumulated the highest
levels of 65Zn in all three species, and rainbow trout gill tissue accumu-
lated less zinc than gill from the other two species. Joyner and Eisler
(1961) immersed Chinook salmon (Oncorhunchus tshauytscha] fingerlings in a
freshwater solution containing 0.2 mg ^5Zn x,"1 for 24 hours followed by
exposure to zinc-free water for 63 days. Fish were then sampled at various
time intervals. Fish accumulated about 2 percent of the zinc present in
the initial test solution and retained almost all of their accumulated zinc
throughout the 63-day period in zinc-free water. However, zinc redistributed
within the fish during the zinc-free portion of the test, increasing in
vertebral column, head and viscera, and decreasing in muscle, skin, scales
and fins. After a seven- to nine-day incubation period, isotopic zinc
injected into the air bladders of goldfish (Cavassius auratus) was accumu-
lated to the largest extent in intestine (Hibiya and Oguri 1961). This
result implies that fish excrete zinc through the intestine.
Three-spined stickleback (Gasterosteus aculeatus) exposed to 65Zn in
freshwater accumulated zinc initially but were then able to reduce their
internal zinc concentration to a level approaching that of control fish
(Matthiessen and Brafield 1977). This unusual ability was attributed to the
euryhaline nature of stickleback. These workers also found that zinc up-
take (whole fish measurements) was higher in water of high hardness even
though zinc toxicity was inversely related to hardness. The authors hy-
pothesized that the low uptake of zinc in calcium-free water could be due
to zinc precipitation of mucus on body surface and gills, with release
into the water. They suggested that zinc toxicity is lower in hard water
because calcium interferes with the internal mechanism of zinc toxicity,
perhaps by occupying potential zinc-binding sites on proteins.
61
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Marafante (1976) found that intraperitoneally injected zinc, mercury and
cadmium were incorporated into the cadmium-binding proteins present in the
livers and kidneys of goldfish (Carassius awatus). All of the cadmium in
liver and kidney was associated with this protein. However, only 40 percent
of the zinc and 17 percent of the mercury in liver and 1.9 percent of the
zinc and 12 percent of the mercury in kidney were associated with the
cadmium-binding protein. The rest was attached to higher molecular weight
proteins. The very low percentage of zinc associated with cadmium-binding
proteins in kidney compared to liver suggests that a specific zinc-binding
protein may exist in this organ.
Wedemeyer (1968) studied the physiology of 65Zn accumulation in coho
salmon (Onaorhynchus kisutch) eggs. Of the 65Zn accumulated, 70 percent
was in the chorion, 26 percent in the perivitelline fluid, 2 percent in the
yolk and 1 percent in the embryo. Ten minutes was required for the yolk to
reach maximum zinc concentration and the level attained was a direct func-
tion of exposure magnitude. Changing pH greatly influenced zinc accumula-
tion by the chorion and perivitelline fluid, with eggs accumulating the
most zinc over the pH range 4 to 9. Exposure to iodoacetate increased zinc
uptake by the perivitelline fluid but did not influence accumulation by
yolk or embryos thus suggesting that the vitelline membrane was not altered.
The mechanism of this increased uptake was believed to be an increased
diffusion of zinc across the chorion, resulting from reduced zinc binding
to the chorion due to a sulfhydryl blockage. Azo dye and malachite green
also increased zinc permeability, but with these chemicals yolk accumulated
substantial amounts of'zinc suggesting that the vitelline membrane had been
altered. The author speculated that the pH dependence of chorion zinc
uptake and the influence of iodoacetate on accumulation suggests that
negative charge groups participate at zinc-binding sites on the chorion.
The fact that an amino blocking agent (2,4-dinitrofluorobenzene) had no
influence on uptake supports this supposition. When copper was present at
concentrations below 2 mg Cu A"1, zinc uptake was inhibited, but above this
concentration zinc uptake was stimulated. Wedemeyer concluded that the
uptake process involves first a physicochemical sorption onto the chorion
along with a passive diffusion of zinc into the perivitelline fluid, yolk
and embryo. Chemicals acting to decrease zinc binding at the chorion
increase diffusion by causing a greater concentration gradient and there-
fore should increase toxicity.
Spehar (1976) exposed flagfish (Jordanella floridae) to various zinc
concentrations in water and observed significant uptake at concentrations
exceeding 47 yg SL~I. Fish reached a plateau level of zinc in less than 30
days. The lowest zinc concentration having an adverse effect on the fish
(reduced growth in females) was 51 yg xr1, indicating that adverse symptoms
are first realized near the metal concentration where accumulation begins
to occur.
Mount (1964) developed an autopsy technique for fish killed from acute
exposure to zinc. The technique utilized the principle that zinc accumu-
lates in opercular bone very slowly regardless of the magnitude of exposure,
whereas gill tissue accumulates zinc at a modest rate during chronic expo-
sures but rapidly during acutely lethal exposures. Thus, the opercular
62
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bone-zinc to gill-zinc ratio proved to be a useful tool for detecting acute
fish mortality due to zinc. Of more than 20 fish species examined from
zinc-pollution-free natural waters, only carp (Cyprinus aarpio} had gill to
opercular bone zinc ratios that precluded the use of this technique.
Previous exposure to sublethal concentrations of zinc did not influence the
usefulness of the method; also, dead fish placed in zinc-contaminated water
gave negative results when analyzed. The validity of this technique was
further confirmed by Cairns et aj_. (1971) who analyzed tissues from adult
bluegill (Lepomis maaroehirusT of various sizes that had undergone acute
zinc exposure under a variety of experimental conditions. These workers
detected zinc above the designated threshold level in some zinc-exposed
survivors; however, this finding was attributed to the fact that these
bluegills were very near death.
Radiozinc uptake by pumpkinseed sunfish (Lepomis gibbosus) from a
natural and a synthetic diet were compared by Merlini ejt al_. (1976). In
addition, zinc uptake from food was compared to that from water. Zinc-65
was accumulated much more readily from an artificially prepared diet than
from a natural diet (the snail Viviparus ater). Both diets contained
similar levels of zinc. After 25 days of feeding, the fish fed the arti-
ficial diet contained nearly six times more zinc than the snail-fed fish.
Moreover, the kind of diet influenced zinc accumulation from water. Fish
fed uncontaminated synthetic diet accumulated three times as much zinc from
water as fish fed snails. This difference in uptake of zinc from water
was believed to be a function of the degree to which the zinc was organically
bound. In fish fed the artificial diet, zinc was available in the ionic
form; in natural food the zinc was more apt to be organically bound and
this was believed to be dependent upon whether the food organism was in the
process of accumulating or eliminating zinc at the time it was eaten. This
hypothesis is consistent with zinc elimination studies which show different
half-times of elimination from different zinc pools within an organism.
Renfro et^ al_. (1975) designed experiments to determine the relative impor-
tance of food and water as sources of 65Zn to fish (Gobius), crabs (Carcinus
maenas) and benthic shrimp (Lysmata seticaudata). Test organisms were
exposed to the isotope only through water or via both routes. Shrimp and
crabs received a lower percentage increment of 65Zn from food than did
fish. At the end of these experiments the final proportions of 65Zn activity
accumulated from food and water and from water alone were approximately
54:45 in shrimp, 71:31 in crabs and 4:1 in fish. However, it should be
noted that the relative ratio of the concentrations of zinc in water and in
food was arbitrarily chosen; the results would obviously change with any
alteration of this ratio. On the average, crabs lost 61 percent of their
zinc activity during molting and shrimp lost 45 percent. Interestingly,
the mode of °5Zn accumulation by the food organism (Artemia salina) of
shrimp did not affect 65Zn uptake by the shrimp. Whole-body concentration
factors after 90 days for the organisms exposed to 65Zn via both food and
water were 380 for shrimp, 210 for crabs and 25 for fish.
Bryan (1967) studied zinc regulation in the freshwater crayfish
(Austropotcmobius palUpes pallipes] to determine if the trend towards
higher zinc blood levels observed in decapod crustaceans in moving from
marine to estuarine types continued into freshwater. However, freshwater
63
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crayfish were found to accumulate lower zinc blood concentrations than
either marine or estuarine forms. Interestingly, this crayfish accumulated
much higher zinc levels in muscle than did its estuarine or marine relative.
The latter finding suggests that crayfish regulated zinc in muscle. High
zinc levels in stomach fluids imply that food is a major route of zinc
uptake. The hepatopancreas was believed to be the principal zinc-regulating
organ. In the marine lobster Homarus vulgaris, Bryan (1964) found that
excretory organs, hepatopancreas and gill increased in zinc concentration
following exposure to zinc through either water or food, but muscle and
gonad remained the same, Zinc was removed from circulation by both hepato-
pancreatic absorption and urinary excretion. Zinc concentration factor was
inversely related to its concentration in water. Zinc was not accumulated
as readily as copper.
Other workers have also reported on zinc's accumulation in and influ-
ence on marine organisms, Scott (1977) compared the mercury and zinc con-
centrations in cleithrum bones from recently caught Atlantic cod (G-adus
morhua) to the content of these metals in cleithra from cod recovered from
an 1865 shipwreck. The historical, fish had mercury concentrations similar
to those in recently collected fish, but the zinc concentration was higher
in the contemporary fish suggesting that the zinc content of the oceans may
be increasing. Wright (1976) found unusually high levels of zinc in fishes
collected off the northeast coast of England*although no known sources of*'
zinc existed in the area. Some individuals were found to contain more than
100 yg Zn g"1 in axial muscle tissue.
Seymour (1966) measured 65Zn uptake in Pacific oysters (Crassostvea
gigas) transferred from radionuclide-free water in Puget Sound to Willapa
Bay, Washington, located just north of the confluence of the Columbia River
with the Pacific Ocean. Cooling water from the Hanford nuclear reactor
containing trace amounts of 65Zn flows down the Columbia River reaching
this portion of the Washington coast. Uptake became asymptotic after 500
days with a final concentration factor of 1.5 x lO4. Zinc-65 elimination
.rate was measured by transferring oysters in the opposite direction. Upon
transfer to uncontaminated water, elimination proceeded linearly with the
biological half-time calculated to be 255 days. Similarly, Osterberg
(1962) was able to detect elevated 65Zn concentrations in euphausiids
(Euphausia paaifioa] and tunicates (Salpa spp.) collected within the
Columbia River plume off the Oregon coast. Wolfe (1970) measured zinc
distribution in South Carolina coastal oysters (Crassostrea virginica).
Although zinc was present throughout the oyster, those tissues with exposed
surfaces such as gills and mantles had the highest concentrations. In
eastern oysters (C. virginiaa), hard-shell clams (Venus mercenaria), and
bay scallops (Pecten irradians) collected near Beaufort, North Carolina,
labial palps and gill accumulated1 the highest levels of zinc whereas adduc- ••
tor muscle was very low (Chipman ejt aj_. 1958). Oysters collected from un-
contaminated areas contained 0.3 to 1.0 vtg Zn g"1, supposedly representing
background levels; clams and scallops contained less zinc than oysters.
Studying the distribution of 65Zn administered to artificial estuarine
ponds, Duke et_ al_. (1966) and, Duke. (1967) noted that eastern oysters,
scallops (Aquipeeten irradians) and clams (Meraenaria mercenaria) accumu-
lated significantly higher levels of the isotope than other organisms
64
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including fish; oysters and clams had the highest concentrations in edible
portions. Sediment acted as a sink for 65Zn in the ponds; over 99 percent
of the 65Zn was in the sediment 100 days after application. Shuster and
Pringle (1969) subjected American eastern oysters to either 0.1 or 0.2 mg
Zn jr1 for up to 20 weeks and compared the zinc levels attained to zinc
levels found in oysters collected along the Atlantic coast of the United
States (Pringle e_t a_l_. 1968). After 20 weeks the experimental oysters
exposed to the two zinc levels averaged about 2650 and 3500 yg Zn g"1
respectively. Comparatively, collected oysters ranged from 204.4 to 4120
yg Zn g"1. These values are much higher than those reported earlier by
Chipman and coworkers (1958).
A large percentage of the 65Zn accumulated by common shrimp (Crangon
crangon) was present in exoskeleton and was, therefore, lost during molting
(van Weers 1975). Increasing the water temperature increased the frequency
of molting, thereby increasing the rate of zinc elimination. Elimination
appeared to be from two compartments. Changing the water temperature from
10 to 15 C resulted in the biological half-time for the slow compartment
decreasing from 33.7 to 16.5 days. In experiments with the salt marsh
snail (Littorina irrorata], 65Zn elimination rate was shown to be directly
related to water temperature and inversely related to snail body size
(Mishima and Odum 1963). Elimination was characterized by a short rapid
phase followed by an extended slower phase; metabolic rate was believed to
be the most important factor regulating zinc elimination rate.
Kameda e_t al_. (1968) measured 65Zn uptake by various organs and tissues
from two marine fishes including marine goby (Chasmichthys gulosus) and
filefish (Rudarius eraodes], a mussel (Mytilus edulis), short-necked clam
(Tapes japonica) and a sea urchin (Strongylocentrotus pulcherrimus). Fish
reached highest zinc concentration in digestive tract, gill and viscera;
muscle and vertebrae accumulated very little zinc. Clams accumulated
highest levels in gill and mantle, but mussels had highest zinc concentra-
tions in adductor muscle, viscera and shell. Mussels accumulated consider-
ably more 65Zn than clams. The digestive tract of the sea urchin contained
much higher zinc levels than its other organs.
In the plaice (Pleuronectes platessa) orally administered 65Zn was
retained at relatively high concentrations by most organs tested including
heart, spleen, liver, kidney, gonad, gut, gill and skin (Pentreath 1973).
Gonads from males were particularly high in zinc, containing approximately
three-times as much zinc as other organs. The biological half-time for
zinc accumulated from water was 313.1 days while intraperitoneally injected
zinc had a half-time of only 210.7 days. Zinc-65 was assimilated almost
twice as efficiently from gelatin or starch pellets compared to 65Zn fed
in live Nereis which had previously been exposed to the isotope. Croaker
(Miaropogon undulatus] fed zinc accumulated high zinc levels in gill, kid-
ney, liver and spleen (Chipman e_t al_. 1958). Upon return to zinc-free
water, most zinc was quickly eliminated.
Eisler (1967) exposed adult mummichog (Fundulus heteroclitus) under
static conditions in saltwater to various zinc concentrations ranging from
0.78 to 180 mg ir1 (these levels bracketed acutely lethal concentrations)
65
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and measured zinc concentrations in gill arch and whole fish after various
exposure intervals. After 192 hours all fish exposed to 42 mg In jr1 or
less survived and contained no more detectable zinc than controls, whereas
all fish exposed to 157 and 180 mg Zn a~l died within 48 hours and contained
on the average seven times as much zinc as control individuals for whole
fish and eight times as much in gill arch. In another study Eisler and
Gardner (1973) exposed mummichog to various combinations of cadmium, copper
and zinc in seawater with several interesting findings. Low levels of
cadmium inhibited zinc accumulation, whereas copper and zinc increased
cadmium accumulation. Dead fish immersed in solutions of zinc or copper
accumulated more metal than living individuals. Similarly, Eisler (1971)
found that dead fish accumulated more cadmium than survivors. These find-
ings should be carefully considered by those interested in using autopsy
indices for determining the cause of fish kills in saltwater.
Hoss (1964) exposed three species of flounder of the genus Paralichthys
to 65Zn added to both food and water. Major conclusions were that zinc
uptake from water was proportionally related to the zinc concentration in
water and zinc uptake from food and water were additive. Nearly 20 percent
of the dietary zinc and 0.2 percent of the aqueous zinc were accumulated;
however, fish were exposed to a static test solution containing a fixed
volume. The percentage of zinc accumulated from water might well vary with
a change in either of these conditions. Accumulation from water would be
more meaningfully related to respiratory volumes. Moreover, food consump-
tion rates were not measured, making comparisons of zinc accumulated from
food and water difficult.
Zinc is readily accumulated by both marine and freshwater fishes from
both food and water, but internal organs and bones accumulate much higher
zinc levels than edible muscle tissue. The time required for fish to reach
threshold levels of zinc appears to be dependent upon species and the chemi-
cal nature of the environment. Upon entering fish some zinc associates with
cadmium-binding proteins and evidence suggests that a zinc-binding protein
may exist. The level at which zinc becomes chronically toxic is very near
the concentration at which zinc begins to accumulate. However, the acute
toxicity of zinc to sticklebacks has been shown to decrease with increasing
calcium concentration even though calcium stimulates zinc uptake. In
marine fishes cadmium reportedly decreases zinc accumulation. Zinc accumula-
tion in salmon eggs has been shown to be a diffusion rate process which can
be altered by chemical factors that influence the diffusion gradient at the
egg membrane surfaces. Because gill tissue accumulates zinc much more
rapidly than bony tissue, a method for detecting zinc-caused fish mortalities
has been developed utilizing the ratio of zinc in gill to zinc in opercular
bone. This technique has proved valid for a variety of fish species.
The zinc content of the oceans appears to be increasing in time. Al-
though marine fishes readily accumulate zinc, evidence suggests that upon
return to zinc-free water marine fishes eliminate zinc much more rapidly
than freshwater fishes. This occurrence may be due to the different osmo-
regulatory problems encountered by fishes in these two environments. Oys-
ters are particularly adept at accumulating zinc, showing concentration
66
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factors as high as 26,500. The half-life of zinc in oysters is reportedly
255 days. Although orally ingested zinc has a low toxicity to humans,
oysters should probably be monitored in areas where zinc contamination is
severe.
67
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SECTION XXIV
GENERAL
Many papers deal largely with the concentrations of groups of metals
found in fishes or other aquatic animals from specific geographic regions,
or with the role played by specific groups of organisms in transporting or
mobilizing metals in general. Many of the conclusions drawn from these
studies were broad in nature and, therefore, were not appropriately applied
to a particular metal. However, some of the conclusions from some of these
papers did apply to a specific metal and when this occurred, the results
were also included in the individual metal section.
long e_t aL. (1974) measured the concentrations of 36 metals in tissue
homogenates from various aged lake trout (Salvelinus namayeush) from Lake
Cayuga, New York. Of all the metals analyzed, chromium concentration in-
creased with fish age while molybdenum decreased1. No age-related trends
were apparent for the other 34 metals. Lucas ejt al_. (1970) measured con-
centrations of 15 metals in liver or muscle of spottail shiner (Notropis
hudsonius), alewife (Alosa pseudoharengus) and trout-perch (Percopsis
omiscomayaus) from Lakes Michigan, Superior and Erie. In addition, various
other Great Lakes fishes were analyzed for selected metals. Small sample
sizes and the absence of information permitting correlation of concentra-
tion with fish size (age) make the data difficult to interpret. However,
a general understanding of the then current levels of some metals in Great
Lakes fishes was derived. Kelso and Frank (1974) also surveyed Lake Erie
fishes including yellow perch (Perca flavesoens), white bass (Morone
chrysops) and smallmouth bass (Micropterus dolomieui) for their cadmium,
copper and mercury contents. Metals occurred at low levels in all species
except for two specimens of white bass which exceeded 0.5 pg Hg g"1.
Results were similar to those reported by Lucas et^ a]_. (1970) for these
three metals.
The Wisconsin Department of Natural Resources (1974) collected fish
from various Wisconsin waters to determine the arsenic, cadmium, chromium,
lead and zinc contents of edible portions. Cadmium was not detectable in
any of the samples but zinc was present at concentrations ranging from 3.0
to 18.3 yg Zn g-1. Arsenic, chromium and lead were for the most part .
present at concentrations less than-1.0 pg g"1-. The authors concluded
that consumption of these fish should not result in any adverse effects on
humans. In Iowa, Morris e_t a]_. (1972)'surveyed fishes from various waters
for their metals contents. Fishes from the Iowa River contained mercury
levels exceeding the FDA guide!ine; but fishes .from all other rivers sur-
veyed contained permissible mercury levels. Other metals, including barium,
68
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cadmium, chromium, copper, lead, nickel and zinc were present at relatively
low concentrations in all samples analyzed.
Uthe and Bligh (1971) compared the concentrations of 13 metals in
dressed fish collected from several industrialized lakes with those in fish
from pristine lakes in Canada and found that, except for mercury, differences
were slight. However, Brown and Chow (1977) compared cadmium, copper,
lead, mercury and zinc levels in fish from a polluted area of Lake Huron
with those in fish from a relatively unpolluted area and found that all
metals were present at higher concentrations in fish from the polluted
area. The ratio between metal concentration in kidney or liver and metal
concentration in muscle was higher in fish from the polluted area for all
metals analyzed. Likewise, Atchison (1975) analyzed warmwater fishes from
an industrialized Indiana lake for cadmium and chromium and reported levels
exceeding those reported for more pristine areas. During a similar study
in Wales (Trollope and Evans 1976) the metals content of algae was shown to
increase moving nearer to a zinc smelter emitting large amounts of metals
wastes. For the metals analyzed the order of concentration factor was
highest for iron followed in decreasing order by zinc, lead, copper arid
nickel. Likewise, fish collected near industrialized areas of England's
Medway estuary contained slightly higher levels of lead and cadmium than
organisms from undeveloped areas (Wharfe and Van Den Broek 1977). Stapleton
(1968) analyzed various tissues'from calico bass (Paralabrax clatkratus}
collected near Los Angeles. Some of the bass were collected from the
pollution-free Catalina Island area and others were collected near the
effluent pipe from a local steam plant. Aluminum, cadmium and nickel were
present at higher levels in fish collected near the steam plant and the
livers from these fish were enlarged. However, none of the metals present,
including cadmium, copper, lead, mercury and zinc, was found at levels
considered to be hazardous.
Mathis and Cummings (1973) measured cadmium, chromium, cobalt, copper,
lead, lithium, nickel and zinc levels in various biotic and abiotic com-
ponents of the Illinois River system. For all metals analyzed, sediment
and animals living in or on the sediment such as clams and tubificid worms
contained higher metals concentrations than either omnivorous or carnivorous
fish. Water contained the lowest concentrations of all metals except
lithium of any of the components analyzed. The partitioning of cadmium,
lead, mercury and thallium in a eutrophic Illinois lake was also studied
(Mathis and Kevern 1975). Thallium was present only in sediment, and
mercury was present in only fish and sediment. The other two metals were
found in all components analyzed including water, sediments, plants, plank-
ton and fish. The feces of migratory waterfowl were also analyzed and were
found to contain high levels of cadmium and lead; the authors suggested
that waterfowl contribute significant amounts of lead and cadmium to this
letke. In another partitioning study Enk and Mathis (1977) looked at the
distribution of cadmium and lead in a small Illinois stream. Both metals
increased in the order: water, fish, sediment, invertebrates. Aquatic
insects contained the highest cadmium levels, and snails contained the most
lead. The association of insects and snails with the sediment was believed
to contribute to their body burden of these metals.
69
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Patrick and Loutit (1976) investigated the transport of various metals
including chromium, copper, iron, lead, manganese and zinc through a food
chain consisting of metal-enriched sediment, bacteria and tubificid worms.
The system studied was a New Zealand river receiving large amounts of
domestic and industrial waste. Results confirmed the hypothesis that these
elements are concentrated as they move through this type of food chain.
Berner e_t aj_. (1962) measured the gamma activity in various marine zooplank-
ton collected from the Pacific Ocean. No attempt was made to distinguish
among isotopes. A general trend was noted between level of radioactivity
(i.e., uptake of fission products) and the animals' feeding method.
Ciliary and mucous filter feeders contained the most radioactivity, followed
in decreasing order by seta! filterers, rapacious forms and tentacular
feeders. Goettl et a]_. (1971) collected aquatic insects from Colorado
streams located near mining and milling sites and analyzed them for copper,
lead and zinc content; orders of insects analyzed included Diptera,
Ephemeroptera, Plecoptera and Trichoptera. On a dry weight basis, insects
were found to contain up to 6440, 6000, and 10,250 yg g~* of copper, lead,
and zinc, respectively. The authors suggested that these high metals levels
might be harmful to fish ingesting these insects.
Giesy and Wiener (1977) studied the frequency distributions of cadmium,
chromium, copper, iron and zinc in whole body homogenates from several
freshwater fish species collected from a South Carolina pond. Essential
elements including copper, iron and zinc were distributed normally, but
non-essential elements such as cadmium and chromium showed a positively
skewed lognormal distribution. These results suggest that the statistical
procedures used to describe normally distributed populations should not be
applied during certain studies of metals accumulation.
Lee and Wilson (1974) looked at the relationship between the water
levels of calcium, magnesium and strontium in various Wisconsin lakes and
the composition of clam shells (Lampsilis siliquoidea vosacea] from these
lakes. No correlation was found, suggesting that factors governing the
immediate environment of the clams influence the relationship. Similarly
in the marine environment Pi 1 key and Goodell (1963) examined the relation-
ship between salinity, temperature and the metals composition (including
barium, iron, magnesium, manganese and strontium) of various marine mollusc
shells. Although some relationships were found, correlations were highly
variable among species. The environmental conditions determining mollusc
shell composition were probably more complex than this study was designed
to elucidate.
Abdullah ejt a]_. (1976) analyzed scales from Atlantic salmon (Salmo
salar] smolts and brown trout (S. trutta] collected from various locations
in the River Dovoy and Lake Bala in North Wales, for manganese and zinc.
Scale manganese and zinc concentrations were compared with concentrations
of these metals in water; it was found that there was a direct linear
relationship, suggesting that the metals levels in scales reflect environ-
mental exposure. Also in Wales, Ireland and Wootton (1977) measured
copper, lead, manganese and zinc concentrations in two marine gastropods
(Littorina Httovea and Thais lapillus) collected from various coastal
locations. Whole body levels of copper, lead and zinc were higher in
70
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Littorina but manganese was present at higher concentrations in Thais.
Digestive gland contained the highest concentrations of copper, manganese
and zinc for both species but shell contained the highest level of lead.
Shell also contained high manganese levels in littorina. Differences in
metals accumulation patterns between the two species were believed to
result from different diets or preferential accumulation of a particular
metal by one species. Papadopoulou et a]_. (1976) measured metals levels
in echinoderms collected near Greece and calculated concentration factors.
Metals whose radioisotopes will become more common as nuclear power
installations become more widespread, including antimony, cesium, chromium,
cobalt, iron, rubidium, scandium, selenium and silver, were intentionally
chosen. Interestingly, specific species of echinoderms showed preferen-
tial propensities for specific metals. The authors suggested that these
"metals specific species" would be good indicator organisms for the par-
ticular metal they favored. Bowness and Morton (1952) measured copper
and zinc concentrations in various portions of the eyes from frogs (Rana
esculenta and R. temporaria.} and fish (Peraa fluviatilis and Salmo trutta).
Both metals were present at very high concentrations in eye tissue from
these animals with the pigment-protein portion of the eye having the
highest concentrations.
Aquatic animals from the Danube River and Danube Canal in Vienna,
Austria, were found to contain only background levels of antimony, chromium,
cobalt, iron, selenium and zinc (Rehwoldt et al. 1975). In carp (Cyprinus
oarpio] from this same river Rehwoldt et aTT TT976) examined the tissue
distributions of chromium, cobalt, iron, lanthanum, scandium and zinc. The
levels of metals in suspended solids in the water were also measured.
Cobalt, lanthanum and scandium were present at highest levels in bone
whereas the other metals preferentially accumulated in gill, liver and
kidney. The gill metals levels were very similar to the levels in sus-
pended solids, suggesting that the metals were on particles imbedded on the
gill surfaces. Justyn and Lusk (1976) examined the accumulation of uranium
and 226Ra in stream fishes living above or below the outfall from a uranium
mine and mill located in northern Bohemia. Both elements were present at
higher concentrations in fish below the mill. Uranium content of brown.
trout was correlated with age, with uptake remaining nearly linear for the
four year classes of fish sampled. Musculature contained much lower levels
of both elements than did bone or entrails, thus reducing the risk to human
consumers.
The changes in iron, manganese and zinc content of spot (Leiostomus
xanthurus), Atlantic croaker (Micropogon undulatus), pinfish (Lagodon
rhomboides]I, bay anchovy (Anahoa mitohilU) and Atlantic menhaden (Bvevoortia
tyrannus] collected off the coast of North Carolina were measured in relation
to time (Cross and Brooks 1973). Excepting manganese in menhaden, the
metals content of all these species decreased with age. This trend was
attributed in part to the proportionate decrease in size with age of tissues
which tend to accumulate the highest levels of these metals (e.g., gastro-
intestinal tract) and partly to the increased offshore migration tendencies
of older fish.
71
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During another study Cross et^ al_. (1973) looked at the relationship
between age and concentrations of copper, iron, manganese, mercury and
zinc in bluefish (Pomatomus saltatrix], a pelagic fish, and morids
(Antimora rostrata), a bathyl-demersal fish, collected off the North
Carolina coast. For both species, only mercury concentration increased
with age, suggesting that the other metals may be at equilibrium between
the fish and their environment. Childs and-Gaffke (1974) measured cadmium
and lead levels in fillets from groundfish caught off the northern and
southern Oregon coasts. In general fish contained less than 0.10 yg Cd
g"1 and less than 0.20 yg Pb g"1. Fish from the northern portion of the
coast contained on the average slightly higher concentrations of both'
metals. Windom e_t aJL (1973) compared arsenic, cadmium, copper, mercury
and zinc levels in several inshore and offshore species of fish from the
North Atlantic. No significant differences were found between fish from
the two areas; however, cadmium, copper and zinc levels were inversely
related to position in the aquatic food chain.
Patterson and Settle (1977) measured the distribution of several
metals in albacore, Thunnus alalunga. Cesium", potassium and rubidium were
uniformly distributed.throughout the various organs and tissues but barium,
calcium, lead and strontium were preferentially accumulated by bone. Com-
paring the distribution'of these metals in tun,a with their distribution in
a terrestrial mammal, the martin (Martes canerioana), showed that the metals
were distributed identically in both animals. Similarly, Goldberg (1962)
examined the distribution of several metals in various Pacific tuna.
General trends noted were that the transition elements (copper, manganese,
nickel, zinc) concentrated in internal organs whereas alkaline earths (cal-
cium, strontium) were concentrated in bony tissues. These trends are
similar to those reported by other workers. Havre et^ a]_. (1972) measured
concentrations of six metals in fish from a Norway fjord suspected to be
contaminated from a zinc factory. Levels were found to be higher than in
uncontaminated areas but not as high as was expected. It was suggested
that zinc may inhibit the uptake of other metals. Greig et_ al_. (1976)
found that fish and invertebrates collected near a deep-water disposal
site contained lower concentrations of cadmium, copper, nickel and zinc
than inshore fish. Various marine fishes and algae from the Bay of Haifa
off the Mediterranean coast of Israel contained only background levels of
cadmium, chromium, copper, lead, nickel and zinc (Roth and Hornung 1977).
Leatherland ejt aj_. (1973) found low levels of antimony, arsenic, cadmium,
mercury and zinc in various fishes and invertebrates collected off the
northwest coast of Africa and in the Azores; metals were generally present
at higher concentrations in invertebrates than in fish. Rossi et aJL
(1976) analyzed canned tuna in Italy for metal content and then calculated
the contribution of metals from tuna to the total metals consumed by the
Italian citizenry. Based on the food habits of the average Italian and
the metals content of other dietary constituents, it was determined that
antimony, cesium, chromium, cobalt, iron, mercury, nickel, selenium and
zinc in tuna did not contribute significantly to the total intake of these
metals from other sources.
Watling and Watling (1976a) measured the concentrations of various
metals including cadmium, copper, iron, manganese, nickel, silver and zinc
72
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in three species of oysters (Crassostrea gigas, C. margaritacea and Ostrea
edulis] collected from the Knysna estuary, South Africa. Comparisons of
the metals concentrations found in these oysters with those observed in the
same species from other estuaries led the authors to conclude that this
estuary was relatively pristine. All three species of oysters had similar
metals concentrations. The mean levels for each metal on a dry tissue
basis were (in yg g'1): Ag 1.9 to 6.4, Cd 2.5 to 3.7, Cu 17-38, Fe 57-167,
Mn 2-16, Ni 1.6-1.7, Zn 396-886. The same authors (1976b) collected mussels
(Chovomytilus meridionalis] from Saldanha Bay, South Africa, and measured
their metals content in relation to weight and sex. The absolute amount of
metal increased as mussel weight increased. Interestingly, copper, iron,
manganese and zinc were significantly higher in females than in males
whereas bismuth and lead were present at higher concentrations in males.
Darracott and Watling (1975) have suggested that a variety of molluscs
could serve as metals pollution monitoring organisms for the various bays
and estuaries of South Africa. These organisms were chosen on the basis
of their relative abundance, longevity, size, sedentary nature and metals
concentrating ability.
Thomas (1975) summarized available information on the role of benthos
in transporting, mobilizing and accumulating metals. Conclusions were that
(1) benthic fauna accumulate more metals from water than from sediment,
(2) benthos metabolize and thereby change the chemical form of some metal
compounds, and (3) benthic organisms themselves are not important sources
of metals to fish but benthos may increase the metals content of overlying
waters by disturbing metals concentrated in sediment. Sediment matrix is
also important in determining the availability of metals to aquatic organ-
isms. Luoma and Jenne (1976) studied the availability of silver, cobalt
and zinc to the deposit-feeding marine clam (Maooma baltkica) using various
sediments including organic detritus, biogenic carbonates (crushed clam
shells), synthetic calcium carbonates and iron or manganese oxides.
Hydrous oxide-bound zinc and cobalt were not available to the clam but
silver was readily accumulated in the presence of iron oxides. Conversely,
organic complexes of zinc and cobalt increased the availability of these
metals to the clam whereas silver accumulation was inhibited when the
clams were placed in an organic sediment matrix. All three metals were
readily accumulated from both synthetic and biogenic calcium carbonate type
sediments. Rates of metals accumulation by the clam were directly related
to the characteristic rate of metals desorption from a particular sediment
type.
Martin (1970) collected copepods off the coast of Puerto Rico both
near the surface and at 100 m depth. The concentrations of copper, iron,
manganese, nickel, lead, strontium and zinc were higher in the deep
samples than in the surface samples. Martin postulated that this was
because the larger species collected in deep water were older and molted
less often than the surface specimens because of the inverse relationship
between food availability and depth. The sinking of molted copepod exo-
skeletons was considered to be an important factor in the biogeochemical
cycling of metals in the world's oceans.
73
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REFERENCES
Abdullah, M. I., J. W. Banks, D. L. Miles, and K. T. O'Grady. 1976.
Environmental dependence of manganese and zinc in the scales of
Atlantic salmon, Salmo salar (L.) and brown trout, Salmo trutta (L.).
Freshwater Biol. 6: 161-166.
Abernathy, A. R., and P. M. Cumbie. 1977. Mercury accumulation by large-
mouth bass (Micpopterus salmoides) in recently impounded reservoirs.
Bull. Environ. Contam. Toxicol. 17(5): 595-602.
Ackefors, H. 1971. Mercury pollution in Sweden with special reference to
conditions in the water habitat. Proc. R. Soc. London Ser. B. 177:
365-387.
Adams, E, S. 1975,, Effects of lead and hydrocarbons from snowmobile
exhaust on brook trout (SalveHnus fontinalis]. Trans. Am. Fish. Soc.
104(2): 363-373.
Amiard-Triquet, C., and 0. C. Amiard. 1975. Etude experimentale du
transfert du cobalt 60 dans une chaine trophique marine benthique.
(Experimental study on the transfer of cobalt-60 in a marine benthic
food chain.) Helgol. Wiss. Meeresunters. 27: 283-297. [In French
with English abstract.]
Anderlini, V. 1974. The distribution of heavy metals in the red abalone,
Haliotis rufescens, on the California coast. Arch. Environ. Ccntam.
Toxicol. 2(3): 253-265.
Anderson, W. L., and K. E. Smith. 1977. Dynamics of mercury at coal-fired
power plant and adjacent cooling lake. Environ. Sci. Techno!. 11(1):
75-80.
Annett, C. S., F. M, D'ltri, 0. R. Ford, and H. H. Prince. 1975. Mercury
in fish and waterfowl from Ball Lake, Ontario. J. Environ. Qual.
4(2): 219-222.
Anon. 1971. Trace metals: unknown, unseen pollution threat. Chem. Eng.
News 49(3): 29-30, 33.
Anon. 1974. Action level for mercury in fish and shellfish. Fed. Register
39(236): 42738-42740.
74
-------
Arima, S., and S. Umemoto. 1976. Mercury in aquatic organisms—II.
Mercury distribution in muscles of tunas and swordfish. Bull. Jpn.
Soc. Sci. Fish. 42(8): 931-937.
Aronson, A. L. 1971. Biologic effects of lead in fish. J. Wash. Acad.
Sci. 61(2): 124-128.
Aronson, J. L., M. Spiesman, and A. K. Aronson. 1976. Note on the distribu-
tion of mercury in fish species in three Ohio lakes. Environ. Pollut.
10: 1-7.
Atchison, G. J. 1975. Uptake and distribution of trace metals in fish.
Tech. Rep. No. 73, Purdue Univ. Water Resour. Res. Center, West
Lafayette, Indiana. 21 p.
Baptist, J. P., and T. J. Price. 1962. Accumulation and retention of
cesium137 by marine fishes. Fish. Bull. No. 206, 62: 177-187.
Barnhart, R. A. 1958. Chemical factors affecting the survival of game
fish in a western Colorado reservoir. Colorado Coop. Fish. Res. Unit
Quart. Rep. 4: 25-27.
Beal, A. R. 1974. A study of selenium levels in freshwater fishes of
Canada's central region. Tech. Rep. Ser. No. CEN/T-74-6. Dept.
Environ., Fisheries Mar. Serv., Winnipeg, Man. 14 p.
Benoit, D. A. 1975. Chronic effects of copper on survival, growth, and
reproduction of the bluegill (Lepomis macrochirus). Trans. Am. Fish
Soc. 104(2): 353-358.
Benoit, D. A., E. N. Leonard, G. M. Christensen, and J. T. Fiandt. 1976.
Toxic effects of cadmium on three generations of brook trout (Salvelinus
fontinalis). Trans. Am. Fish. Soc. 105(4): 550-560.
Benson, W. W., W. Webb, D. W. Brock, and J. Gabica. 1976. Mercury in cat-
fish and bass from the Snake River in Idaho. Bull. Environ. Contam.
Toxicol. 15(5): 564-567.
Berg, G. G., and E. Ginsberg. 1976. Partition of ruthenium-106 between the
freshwater environment and crayfish. Health Phys. 30: 329-338.
Berner, L. Jr., R. Bieri, E. D. Goldberg, D. Martin, and R. L. Wisner. 1962.
Field studies of uptake of fission products by marine organisms.
Limnol. Oceanogr. 7(supp.): Ixxxii-xci.
Berry, J. W., D. W. Osgood, and P. A. St. John. 1974. Chemical villains.
A biology of pollution. C. V. Mosby Co., St. Louis, Missouri. 189 p.
Bertine, K. K., and E. D. Goldberg. 1972. Trace elements in clams, mussels,
and shrimp. Limnol. Oceanogr. 17(6): 877-884.
75
-------
Birmingham, D. J., M. M. Key, D. A. Holaday, and V. B. Perone. 1965. An
outbreak of arsenical dermatoses in a mining community. Arch. Dermatol.
91: 457-464.
Bisogni, J. J. Jr., and A. W. Lawrence. 1975. Kinetics of mercury methyla-
tion in aerobic and anaerobic aquatic environments. J. Water PoTlut.
Control Fed. 47(1): 135-152.
Bowness, J. M., and R. A. Morton. 1952. Distribution of copper and zinc in
the eyes of fresh-water fishes and frogs. Occurrence of metals in
melanin fractions from eye tissues, Biochem. J. 51: 530-535.
Braman, R. S., and C. C. Foreback. 1973. Methylated forms of arsenic in
the environment. Science 182: 1247-1249.
Brown, B. E. 1977. Uptake of copper and lead by a metal-tolerant isopod
Asellus meridianus Rac. Freshwater Biol. 7: 235-244.
Brown, J. R., and L. Y. Chow. 1977. Heavy metal concentrations in Ontario
fish. Bull. Environ. Con tarn'. Toxicol. 17(2): 190-195.
Brungs, W. A. Jr. 1967. Distribution of cobalt 60, zinc 65, strontium 85,
and cesium 137 in a freshwater ponct, PiibT. No. 999-RH-24, U.S. Public
Health Service, Washington, D.C. 52 p.
Brungs, W. A., E. N. Leonards and J. M. McKim. 1973. Acute and long-term
accumulation of copper by the brown bullhead, Ictalurus nebulosus. J.
Fish. Res. Board Can, 30(4):'583-586.
Bryan, G. W. 1964. Zinc regulation in the lobster Homarus vulgaris, I.
Tissue zinc and copper concentrations. J. Mar. Biol. Assoc. U.K. 44:
549-563.
Bryan, G. W. 1967. Zinc regulation in the freshwater crayfish (including
some comparative copper analyses). J. Exp. Biol. 46(2): 281-296.
Bryan, G. W. 1971. The effects of heavy metals (other than mercury) on
marine and estuarine organisms. Proc. R. Soc.'London Ser. B. 177:
389-410.
Buhler, D. R., R. M. Stokes, and R. S. Caldwell. 1977. Tissue accumulation
and enzymatic effects of hexavalent chromium in rainbow trout (Salmo
gairdneri). J. Fish. Res. Board "Can. 34(1): 9-18.
Burrows, W. D. 1977. Aquatic aluminum: chemistry, toxicology, and environ-
mental prevalence. CRC Critical Reviews in Environmental Control 7(2):
167-216.
Caines, L. A., and A. V. Holden. 1976. Stream pollution by an organomercury
compound. Bull. Environ. Contam. Toxicol. 16(4): 383-391.
76
-------
Cairns, J., Jr., N. H. Cromer, T. K. Banns, and W. T. Waller. 1971. A con-
firmation of Mount's autopsy technique for zinc-caused fish mortality.
Water Resour. Bull. 7(5): 956-968.
Cairns, J., Jr., T. K. Banns, D. T. Burton, K. L. Dickson, R. E. Sparks, and
W. T. Waller. 1972. The effects of pH, solubility and temperature upon
the acute toxicity of zinc to the bluegill sunfish (Lepomis maafoohivus
Raf.). Trans. Kansas Acad. Sci. 74(1): 81-92.
Calabrese, A., F. P. Thurberg, M. A. Dawson, and D. R. Wenzloff. 1975. Sub-
lethal physiological stress induced by cadmium and mercury in the winter
flounder, Pseudopleuronectes americanus. Pages 15-21 In: Sublethal
effects of toxic chemicals on aquatic animals, J. H. Koeman and J. J. T.
W. A. Strik (Eds.), Elsevier Sci. Pub. Co., Amsterdam.
Cearley, J. E. 1971. Toxicity and bioconcentration of cadmium, chromium,
and silver in Miaropterus salmoides and Lepomis macrochirus . Ph.D.
Thesis, Univ. Oklahoma, Norman, 84 p; Diss. Abstr. 32B: 5281-B (1972).
Cearley, J. E., and R. L. Coleman. 1974. Cadmium toxicity and bioconcen-
tration in largemouth bass and bluegill. Bull. Environ. Contam.
Toxicol. 11(2): 146-151.
Chakoumakos, C. 1977. The toxicity of copper to rainbow and cutthroat
trouts under different conditions of alkalinity, pH, and hardness.
M.S. Thesis, Univ. Wisconsin, Madison. 47 p.
Chappell, W. R. 1975. Transport and biological effects of molybdenum in
the environment. Pages 167-192 In: Heavy metals in the aquatic en-
vironment, P. A. Krenkel (Ed.), Pergamon Press, Oxford.
Childs, E. A., and J. N. Gaffke. 1973. Mercury content of Oregon ground-
fish. Fish. Bull. 71(3): 713-717.
Childs, E. A., and J. N. Gaffke. 1974. Lead and cadmium content of selected
Oregon groundfish. J. Food Sci. 39: 853-854.
Chipman, W. A., T. R. Rice, and T. J. Price. 1958. Uptake and accumulation
of radioactive zinc by marine plankton, fish, and shellfish. Fish.
Bull. 135: 279-292.
Chipman, W. A. 1967. Some aspects of the accumulation of 51Cr by marine
organisms. Pages 931-941 In: Radioecology concentration processes,
B. Aberg and F. P. HungateTEds.), Pergamon Press, New York.
Chow, T. J., C. C. Patterson, and D. Settle. 1974. Occurrence of lead in
tuna. Nature 251(5471): 159-161.
Chow, T. J., H. G. Snyder, and C. B. Snyder. 1976. Mussels (Mytilus sp.)
as an indicator of lead pollution. Sci. Total Environ. 6: 55-63.
77
-------
Clubb, R. W., A. R. Gaufin, and J. L. Lords. 1975. Acute cadmium toxicity
studies upon nine species of aquatic insects. Environ. Res. 9: 332-341.
Coleman, R, L., and J. E. Cearley. 1974. Silver toxicity and accumulation
in largemouth bass and bluegill. Bull. Environ. Contam. Toxicol. 12(1):
53-61.
Cooper, C. F., and W. C. Jolly. 1970. Ecological effects of silver iodide
and other weather modification agents: A review. Water Resour. Res.
6(1): 88-98.
Cox, M. F., H. W. Holm, H. J. Kania, and R. L. Knight. 1975. Methylmercury
and total mercury concentrations in selected stream biota. Pages 151-
155 In: Trace substances in environmental health-IX, D. D. Hemphill
(Ed.77 Univ. Missouri, Columbia.
Crockett, A. B., G. B. Wiersma, H. Tai, and W. Mitchell. 1975. Pesticide
and mercury residues in commercially grown catfish. Pestic. Monit. J.
8(4): 235-240.
Cross, F. A., and J. H. Brooks. 1973. Concentrations of manganese, iron,
and zinc in juveniles of five estuarine-dependent fishes. Pages 769-
775 Jjr. Radionuclides in Ecosystems, Vol. 2., D. J. Nelson (Ed.),
USAEC CONF-710501-P2, Springfield, Virginia.
Cross, F. A., L. H. Hardy, N. Y. Jones, and R. T. Barber. 1973. Relation
between total body weight and concentrations of manganese, iron,
copper, zinc, and mercury in white muscle of bluefish (Pomatomus
saltatrix) and a bathyl-demersal fish Antimora rostrata. J. Fish.
Res. Board Can. 30(9): 1287-1291.
Cugurra, F., and G. Maura. 1976. Mercury content in several species of
marine fish. Bull. Environ. Contam. Toxicol. 15(5): 568-573.
Cumbie, P. M. 1975. Mercury levels in Georgia otter, mink and freshwater
fish. Bull. Environ. Contam. Toxicol. 14(2): 193-196.
Dabrowski, K. R. 1976. The effect of arsenic on embrional development of
rainbow trout (Salmo gairdneri Rich.). Water Res. 10: 793-796.
Darracott, A., and H. Watling. 1975. The use of molluscs to monitor cad-
mium levels in estuaries and coastal marine environments. Trans. R.
Soc. S. Afr. 41(4): 325-338.
Dethlefsen, V., H. von Westernhagen, and H. Rosenthal. 1975. Cadmium up-
take by marine fish larvae. Helgol. Wiss. Meeresunters. 27: 396-407.
D'ltri, F. M. 1972. Mercury in the aquatic ecosystem. Tech. Rep. No. 23,
Inst. Water Res., Michigan State Univ., East Lansing. 101 p.
78
-------
Doi, R., and J. Ui. 1975. The distribution of mercury in fish and its
form of occurrence. Pages 197-221 In: Heavy metals in the aquatic
environment, P. A. Krenkel (Ed.), Pergamon Press, Oxford.
Doudoroff, P., and M. Katz. 1953. Critical review of literature on the
toxicity of industrial wastes and their components to fish. II. The
metals, as salts. Sewage Ind. Wastes 25(7): 802-839.
Duke, T. W., J. N. Willis, and T. 0. Price. 1966. Cycling of trace ele-
ments in the estuarine environment. I. Movement and distribution of
zinc 65 and stable zinc in experimental ponds. Chesapeake Sci. 7(1):
1-10.
Duke, T. W. 1967. Possible routes of zinc 65 from an experimental estuarine
environment to man. J. Water Pollut. Control Fed. 39(4): 536-542.
Eaton, J. G. 1974. Chronic cadmium toxicity to the bluegill (Lepomis
macroohirus Rafinesque). Trans. Am. Fish. Soc. 103(4): 729-735.
Eganhouse, R. P., and D. R. Young. 1976. Mercury in tissues of mussel off
southern California. Mar. Pollut. Bull. 7(8): 145-147.
Eisler, R. 1967. Acute toxicity of zinc to the killifish, Fundulus
hetevoclitus. Chesapeake Sci. 8(4): 262-264.
Eisler, R. 1971. Cadmium poisoning in Fundulus heteroclitus (Pisces:
Cyprinodontidae) and other marine organisms. J. Fish. Res. Board Can.
28(9): 1225-1234.
Eisler, R., G. E. Zaroogian, and R. J. Hennekey. 1972. Cadmium uptake by
marine organisms. J. Fish. Res. Board Can. 29(9): 1367-1369.
Eisler, R., and G. R. Gardner. 1973. Acute toxicology to an estuarine
teleost of mixtures of cadmium, copper and zinc salts. J. Fish Biol.
5: 131-142.
Eisler, R. 1974. Radiocadmium exchange with seawater by Fundulus
heteroclitus (L.) (Pisces: Cyprinodontidae). J. Fish Biol. 6: 601-612.
Ellis, M. M., B. A. Westfall, and M. D. Ellis. 1941. Arsenic in fresh-
water fish. Ind. Eng. Chem. 33(10): 1331-1332.
Enk, M. D., and B. 0, Mathis. 1977. Distribution of cadmium and lead in a
stream ecosystem. Hydrobiologia 52(2-3): 153-158.
Eyman, L. D., and T. R. Trabalka. 1977. Plutonium-237: Comparative
uptake in chelated and non-chelated form by channel catfish (lotalurus
punotatus). Health Phys. 32(6): 475-478.
o
Fagerstrbm, T., and B. Asell. 1976. Caged fish for estimating concentra-
tions of trace substances in natural waters. Health Phys. 31: 431-
439.
79
-------
Fassett, D. W. 1975. Cadmium: biological effects and occurrence in the
environment. Annu. Rev. Pharmacol. 15: 425-435.
Feldt, W. 1963. Measurement of strontium 90 and caesium 137 in fishes.
Pages 105-111 In: Nuclear detonations and marine radioactivity.
Norwegian Defence Research Establishment, Kjeller, Norway.
Flegal, A. R. 1977. Mercury in the seston of the San Francisco Bay
estuary. Bull. Environ. Contam. Toxicol. 17(6): 733-738.
Flick, D. F., H. F. Kraybill, and J. M. Dimitroff. 1971. Toxic effects of
cadmium: a review. Environ. Res. 4: 71-85.
Fowler, S. W., and G. Benayoun. 1974. Experimental studies on cadmium
flux through marine biota. Pages 159-177 In: Comparative studies of
food and environmental contamination. International Atomic Energy
Agency, Vienna.
Fowler, S., M. Heyraud, and T. M. Beasley. 1975. Experimental studies on
Plutonium kinetics in marine biota. Pages 157-177 In: Impacts of
nuclear releases into the aquatic environment. International Atomic
Energy Ageney, Vienna; / k.
Fowler, S. W., and G. Benayoun. 1976a. Accumulation and distribution of
selenium in mussel and shrimp tissues. Bull. Environ. Contam. Toxicol.
16(3): 339-346.
Fowler, S. W., and G. Benayoun. 1976b. Selenium kinetics in marine zoo-
plankton. Mar. Sci. Commun. 2(1): 43-67.
Freeman, R. A., and W. H. Everhart. 1971. Toxicity of aluminum hydroxide
complexes in neutral and basic media to rainbow trout. Trans. Am.
Fish. Soc. 100(4): 644-658,
Friedrich, A. R., and F. P. Filice. 1976. Uptake and accumulation of the
nickel ion by Mytilus edulis. Bull. Environ. Contam. Toxicol. 16(6):
750-755.
Fromm, P. 0., and R. M. Stokes. 1962. Assimilation and metabolism of
chromium by trout. J. Water Pollut. Control Fed. 34(11): 1151-1155.
Fromm, P. 0. 1977. Toxic effect of water soluble pollutants on freshwater
fish. EPA Ecol. Res. Ser. EPA-600/3-77-057, U.S. Environmental Pro-
tection Agency, Environmental Research Laboratory-Duluth. 53 p.
Gajewska, R., M. Nabrzyski, E. Lipka, and A. Gajewski. 1976. Badania
zawartosci olowiu w rybach morskich i slodkowodnych. (Studies on lead
content in salt and fresh-water fish.) Bromatol. Chem. Toksykol.
9(1): 7-12. [In Polish with English summary.]
Ganther, H. E., and M. L. Sunde. 1974. Effect of tunafish and selenium on
the toxicity of methylmercury: a progress report. J. Food Sci. 39:
1-5.
80
-------
Gavis, 0., and J. F. Ferguson. 1972. The cycling of mercury through the
environment. Water Res. 6: 989-1008.
Gergely, A., K. Soos, L. Erdelyi, and V. Cieleszky. 1977. Determination
of mercury in fish from rivers and lakes in Hungary by atomic absorp-
tion technique. Toxicology 7: 349-355.
Giblin, F. J., and E. J. Massaro. 1975. The erythrocyte transport and
transfer of methylmercury to the tissues of the rainbow trout (Salmo
gairdneri]. Toxicology 5: 243-254.
Giesy, J. P., Jr., and J. G. Wiener. 1977. Frequency distributions of
trace metal concentrations in five freshwater fishes. Trans. Am.
Fish. Soc. 106(4): 393-403.
Gilderhus, P. A. 1966. Some effects of sublethal concentrations of sodium
arsenite on bluegills and the aquatic environment. Trans. Am. Fish.
Soc. 95(3): 289-296.
Goettl, J. P., Jr., J. P. Sinley, and P. H. Davies. 1971. Study of the
effects of mineral mining and milling operations on high mountain
streams. Pages 1-48 In: Water pollution studies. Job Prog. Rep.,
Fed. Aid Proj. F-33-R-6, Colorado Division of Wildlife, Fort Collins,
Colorado.
Goettl, J. P., Jr., J. R. Sinley, and P. H. Davies. 1972. Study of the
effects of metallic ions on fish and aquatic organisms. Baseline
levels of zinc and copper in rainbow trout. Pages 42-45 In: Water
pollution studies. Job Prog. Rep., Fed. Aid Proj. F-33-R-7, Colorado
Division of Wildlife, Fort Collins, Colorado.
Goettl, J. P., Jr., J. R. Sinley, and P. H. Davies. 1974. Water pollution
studies. Job Prog. Rep., Fed. Aid Proj. F-33-R-9, Colorado Division of
Wildlife, Fort Collins, Colorado. 96 p.
Goettl, J. P., Jr., and P. H. Davies. 1977. Study of the effects of metallic
ions on fish and aquatic organisms. Tissue molybdenum levels. Pages
53-61 In: Water pollution studies. Job Prog. Rep., Fed. Aid Proj.
F-33-R-12, Colorado Division of Wildlife, Fort Collins, Colorado.
Goldberg, E. D. 1962. Elemental composition of some pelagic fishes.
Limnol. Oceanogr. 7(supp.): Ixxii-lxxv.
Greig, R. A., A. E. Adams, and B. A. Nelson. 1974. Physiological response
of the cunner, Tautogolabrus adspersus, to cadmium. II. Uptake of
caximium by organs and tissues. NOAA Tech. Rep. NMFS SSRF-681. pp. 5-9.
Greig, R. A., D. R. Wenzloff, and J. B. Pearce. 1976. Distribution and
abundance of heavy metals in finfish, invertebrates and sediments
collected at a deepwater disposal site. Mar. Pollut. Bull. 7(10):
185-187.
81
-------
Greig, R. A., D. Wenzloff, C. Shelpuk, and A. Adams. 1977. Mercury concen-
trations in three species of fish from north Atlantic offshore waters.
Arch. Environ. Contam. Toxicol. 5: 315-323.
Guary, J. C,, M. Masson, and A. Fraizier. 1976. Etude preliminaire, in
situ, de la distribution du plutonium dans differents tissus et organes
de Cancer pagwms (Crustacea:Decapoda) et de Pleuroneetes platessa
(Pisces: Pleuronectidae). (in situ preliminary study of plutonium
distribution in different tissues and organs of Cancer pagurus
(Crustacea:Decapoda) and Pleuroneates platessa (Pisces:Pleuronectidae)).
Mar. Biol. 36: 13-17. [In French with English abstract.]
Guary, J. C., and A. Fraizier. 1977a. Etude comparee des teneurs en
plutonium chez divers mollusques de quelques sites littoraux francais.
(Comparative study of the plutonium levels in various molluscs from
several French littoral sites.) Mar. Biol. 41: 263-267. [In French
with English abstract.]
Guary, J. C., and A. Fraizier. 1977b. Influence of trophic level and cal-
cification on the uptake of plutonium observed, in situ, in marine
organisms. Health Phys. 32: 21-28.
Gustafson, P. F., S. S. Brar, and S. E. Muniak. 1966. Caesium-137 in
edible freshwater fish. Nature 211(5051): 843-844.
Hall, A. S., F. M. Teeny, L. G. Lewis, W. H. Hardman, and E. J. Gauglitz, Jr.
1976a. Mercury in fish and shellfish of the northeast Pacific. I.
Pacific halibut, Bippoglossus stenolepis. Fish. Bull. 74(4): 783-789.
Hall, A. S., F. M. Teeny, and E. J. Gauglitz, Jr. 1976b. Mercury in fish
and shellfish of the northeast Pacific. II. Sablefish, Anoplopoma
fimbria. Fish. Bull. 74(4): 791-797.
Hall, A. S., F. M. Teeny, and E. J. Gauglitz, Jr. 1977. Mercury in fish and
shellfish of the northeast Pacific. III. Spiny dogfish, Squalus
aoanthias. Fish. Bull. 75(3): 642-645.
Hannerz, L. 1968. Experimental investigations on the accumulation of
mercury in water organisms. Fish. Board Swed., Inst. Freshwater Res.,
Drottningholm, Rep. 48: 120-175.
Harrison, F. L. 1973. Availability to .aquatic animals of short-lived
radionuclides from a plowshare cratering event. Health Phys. 24:
331-343.
Hartung, R. 1976. Pharmacokinetic approaches to the evaluation of methyl-
mercury in fish. Pages 233-248 j_n_: Toxicity to biota of metal forms
in natural waters, R. W. Andrew, P. V. Hodson and D. E. Konasewich
(Eds.), Great Lakes Research Advisory Board, International Joint
Commission, Windsor, Ontario.
82
-------
Ha'sa'nen, E., and J. K. Miettinen. 1963. Caesium-137 content of fresh-
water fish in Finland. Nature 200(4910): 1018-1019.
Havre, G. N., B. Underdal, and C. Christiansen., 1972. The content of lead
and some other heavy elements in different fish species from a fjord
in western Norway. Pages 99-111 In_: Proc. Int. Symposium, Environ-
mental Health Aspects of Lead, Amsterdam (Netherlands), October 2-6,
1972.
Havre, G. N., B. Underdal, and C. Christiansen. 1973. Cadmium concentra-
tions in some fish species from a coastal area in southern Norway.
Oikos 24: 155-157.
Heisinger, 0. F., and W. Green. 1975. Mercuric chloride uptake by eggs of
the ricefish and resulting teratogenic effects. Bull. Environ.
Contam. Toxicol. 14(6): 665-673.
HejtmSnek, M., Z. Svobodova, and M. Studnicka. 1975. Total mercury content
in the musculature of fishes from some dam lakes in Bohemia. Acta Vet.
(Brno). 44: 53-58.
Hewett, C. J., and D. F. Jefferies. 1976. The accumulation of radioactive
caesium from water by the brown trout (Salmo trutta) and"its comparison
with plaice and rays. J. Fish Biol. 9: 479-489.
Hibiya, T., and M, Oguri. 1961. Gill absorption and tissue distribution of
some radionuclides (Cr-51, Hg-203, Zn-65 and Ag-llOm. 110) in fish.
Bull. Jpn. Soc. Sci. Fish. 27(11): 996-1000.
Hildebrand, S. G., A. W. Andren, and J. W. Huckabee. 1976. Distribution and
bioaccumulation of mercury in biotic and abiotic compartments of a
contaminated river-reservoir system. Pages 211-232 In: Toxicity to
biota of metal forms in natural water, R. W. Andrew,~T. V. Hodson and
D. E. Konasewich (Eds.), Great Lakes Research Advisory Board, Inter-
national Joint Commission, Windsor, Ontario.
Hodson, P. V. 1975. Zinc uptake by Atlantic salmon (Salmo salar] exposed to
a lethal concentration of zinc at 3, 11, and 19 C. J. Fish. Res. Board
Can. 32(12): 2552-2556.
Holcombe, G. W., D. A. Benoit, E. N. Leonard, and J. M. McKim. 1976. Long-
term effects of lead exposure on three generations of brook trout
(Salvelinus fontinalis). J. Fish. Res. Board Can. 33(8): 1731-1741.
Hoss, D. E. 1964. Accumulation of zinc-65 by flounder of the genus
Paraliahthys. Trans. Am. Fish. Soc. 93(4): 364-368.
Igelsrud, I., T. G. Thompson, and B. M. G. Zwicker. 1938. The boron content
of sea water and of marine organisms. Am. J. Sci. 35(205): 47-63.
83
-------
Ireland, M. P., and R. J. Wootton. 197,7. Distribution of lead, zinc, copper
and manganese in the marine gastropods, Thais • lapillus and Littorina
iittovea* around the coast of Wales. Environ'. Po-llut. 12: 27-41.
Ishak, M. M., S. R. Khalil, and W. E. Y. Abdelmalik. 1977. Distribution
and tissue retention of cesium-134 and cobalt-60 in the Nile catfish
Clarias lazera (Cuv. & Val.}. Hydrobiologia 54(1): 41-48.
Ishikawa, M., T. Koyanagi, and M. Saiki. 1976. Studies on the chemical
behaviour of 106Ru in sea water and its uptake by marine organisms--!.
Accumulation and excretion of 105Ru by clam. Bull. Jpn. Soc. Sci.
Fish. 42(3): 287-297.
Iverson, W. P., C. Huey, F. E. Brinckman, K. L. Jewett, and-'W. Blair. 1975.
Biological and nonbiological transformations of mercury in aquatic
systems. Pages 193-195 In: Heavy metals in the aquatic environment,
P. A. Krenkel (Ed.), Pergamon Press, Oxford.
Jackim, E., G. Morrison, and R. Steele. 1977. Effects of environmental
factors on radiocadmium uptake by four species of marine bivalves.
Mar. Biol. 40: 303-308.
*i ; • '
Jacobs, G. 1977. Gesamt-und organised gebundener Quecksilbergehalt in
Fischen aus deutschen Fanggriinden. (Total and organically bound
mercury content in fishes from German fishing grounds.) Z. Lebensm.-
Unters.-Forsch. 164: 71-76. [In German with English summary.]
Jefferies, D. F., and C. J. Hewett. 1971. The. accumulation and excretion
of radioactive caesium by the plaice (Pleuronectes platessa] and the
thornback ray (Raia clavata}. J. Mar. Biol. Assoc. U.K. 51(2): 411-
422; Sport Fishery Abstr. 16(3): 13814 (1971).
Jelinek, C. F., and P. E. Corneliussen. 1977. Levels of arsenic in the
United States food supply. Environ. "Health Perspec. 19: 83-87.
Jensen, S., and A. Jernelbv. 1969. Biological methylation of mercury in
aquatic organisms. Nature 223: 753-754.
Jernelov, A., and H. Lann. 1971. Mercury accumulation in food chains.
Oikos 22: 403-406.
Jernelov, A., L. Landner, and T. Larsson. 1975. Swedish perspectives on
mercury pollution. J. Water Pollut. Control Fed. 47(4): 810-822.
Jeyachandran, P., and S. P. Raj. 1975. Mercury""in fish from Mettuf
Reservoir. Curr. Sci. 44(22): 828-829.
Jones, R. F. 1960. The accumulation, of nitrosyl ruthenium by fine.particles
and marine organisms. Limnol. Oceanogr.- 5: ^312-325.
F
Joyner, T. 1961. Exchange of zinc with environmental solutions by the
brown bullhead. Trans.-Am. Fish. Soc. 90: 444-448.
. ' . « •• *
84
-------
Joyner, T., and R. Eisler. 1961. Retention and trans!ocation of radio-
active zinc by salmon fingerlings. Growth 25: 151-156.
Justyn, J., and S. Lusk. 1976. Evaluation of natural radionuclide con-
tamination of fishes in streams affected by uranium ore mining and
milling. Zool. Listy 25(3): 265-274.
Kameda, K., M. Shimizu, and Y. Hiyama. 1968. On the uptake of 65Zn and
the concentration factor on Zn in marine organisms. I. Uptake of
65Zn in marine organisms. J. Radiat. Res. 9(2):50-62.
Kauranen, P., and T. Jarvenpaa. 1972. Biological half-times of 210Po and
210Pb in some marine organisms. Annual Rep., Dep. Radiochemistry,
Univ. Helsinki, Finland. 11 p.
Kelly, T. M., J. D. Jones, and G. R. Smith. 1975. Historical changes in
mercury contamination in Michigan walleyes (stizostedion vitreum
vitreum}. J. Fish. Res. Board Can. 32(10): 1745-1754.
Kelso, J. R. M., and R. Frank. 1974. Organochlorine residues, mercury,
copper and cadmium in yellow perch, white bass and smallmouth bass,
Long Point Bay, Lake Erie. Trans. Am. Fish. Soc. 103(3): 577-581.
Kerfoot, W. B., and S. A. Jacobs. 1976. Cadmium accrual in combined waste-
water treatment-aquaculture system. Environ. Sci. Technol. 10(7):
662-667.
Kim, J. H., E. Birks, and J. F. Heisinger. 1977. Protective action of
selenium against mercury in northern creek chubs. Bull. Environ.
Contam. Toxicol. 17: 132-136.
Kinkade, M. L., and H. E. Erdman. 1975. The influence of hardness com-
ponents (Ca2+ and Mg2+) in water on the uptake and concentration of
cadmium in a simulated freshwater ecosystem. Environ. Res. 10(2):
308-313.
Klemmer, H. W., C. S. Unninayer, and W. I. Okubo. 1976. Mercury content of
biota in coastal waters in Hawaii. Bull. Environ. Contam. Toxicol.
15(4): 454-457.
Knapp, C. E. 1971. Beryllium—hazardous air pollutant. Environ. Sci.
Technol. 5(7): 584-585.
Knoll, J., and P. 0. Fromm. 1960. Accumulation and elimination of hexa-
valent chromium in rainbow trout. Physiol. Zool. 33(1): 1-8.
Knbppler, H.-O., and P. Dorn. 1976. Untersuchungen von Slisswasserfischen
auf Quecksilber- und PestizidrUcksta'nde. Arch. Lebensmittelhyg. 27:
23-26. [In German with English summary.]
85
-------
Koeman, J. H., W. H. M. Peeters, C. H. M. Koudstaal-Hol, P. S. Tjioe, and
J. J. M. deGoeij. 1973. Mercury-selenium correlations in marine
mammals. Nature 245(5425): 385-386.
\
Kojima, K., and M. Fujita. 1973. Summary of recent studies in Japan on
methyl mercury poisoning. Toxicology 1: 43-62.
Koli, A. K., W. R. Williams, E. B. McClary, E. L. Wright, and T. M. Burrell.
1977. Mercury levels in freshwater fish of the state of South Carolina,
Bull. Environ. Contam. Toxicol. 17(1): 82-89.
Kopp, J. F.s and R. C. Kroner. 1970. Trace metals in waters of the United
States. Division of Pollution Surveillance, Federal Water Pollution
Control Administration, U.S. Dep. Interior, Cincinnati, Ohio. 28 p +
Appendices.
Kramer, H. J., and B. Neidhart. 1975. The behavior of mercury in the
system water—fish. Bull. Environ. Contam. Toxicol. 14(6): 699-704.
Kr'uger, K. E., L. Nieper, and H.-J. Auslitz. 1975. Bestimmung des
Quecksilber-Gehaltes der Seefische auf den Fangpla'tzen der deutschen
Hochsee- und Klistenfischerei. (Determination of mercury content of
sea fish in fishing ground of German deep sea and inshore fishing.)
Arch. Lebensmittelhyg. 26: 201-207. [In German with English summary.]
Krumholz, L. A. 1956. Observations on the fish population of a lake
contaminated by radioactive wastes. Bull. Am. Mus. Nat. Hist.
110(4): 277-368.
Krumholz, L. A., E. D. Goldberg, and H. Boroughs. 1957. Ecological
factors involved in the uptake, accumulation, and loss of radio-
nuclides by aquatic organisms. Pages 69-79 In: Effects of atomic
radiation on oceanography and fisheries. Nat. Acad. Sci.-Nat. Res.
Counc., Pub. 551, Washington, D.C.
Kudo, A. 1976. Mercury transfer from bed sediments to freshwater fish
(guppies). J. Environ. Qua!. 5(4): 427-430.
Kuhnert, P. M., and B. R. Kuhnert. 1976. The effect of in vivo chromium
exposure on Na/K- and Mg-ATPase activity in several tissues of the
rainbow trout (Salmo gairdneri]. Bull. Environ. Contam. Toxicol.
15(4): 383-390.
Kulikov, N. V., and L. N. Ozhegov. 1975. Accumulation of Co60 by developing
eggs of pike, perch, and whitefish. Soviet J. Ecol. 6(4): 375-376.
Kumada, H., S. Kimura, M. Yokote, and Y. Matida. 1973. Acute and chronic
toxicity, uptake and retention of cadmium in freshwater organisms.
Bull. Freshwater Fish. Res. Lab. Tokyo 22: 157-165.
86
-------
taarman, P. W., W. A. Willford, and J. R. Olson. 1976. Retention of
mercury in the muscle of yellow perch (Peroa flavesoens] and rock bass
(AmblopZites rupestris). Trans. Am. Fish. Soc. 105(2): 296-300.
Laxen, D. P. H., and R. M. Harrison. 1977. The highway as a source of
water pollution: an appraisal with the heavy metal lead. Water Res.
11: 1-11.
Leatherland, T. M., J. D. Burton, F. Culkin, M. J. McCartney, and R. J.
Morris. 1973. Concentrations of some trace metals in pelagic organ-
isms and of mercury in northeast Atlantic Ocean water. Deep-Sea Res.
20: 679-685.
LeBlanc, P. J., and A. L. Jackson. 1973. Arsenic in marine fish and
invertebrates. Mar. Pollut. Bull. 4(6): 88-90.
Lee, G. F., and W. Wilson. 1974. Studies on the Ca, Mg, and Sr content
of freshwater clamshells. Wise. Acad. Sci., Arts and Lett. 62:_..
173-180.
Lehnin.ger, A. L. 1970. Biochemistry. Worth Publishers, Inc., New
York. 833 p. • .
Lofroth, G. 1970. Methylmercury. A review of health hazards and side
effects associated with the emission of mercury compounds into
natural systems. Ecological Res. Comm. Bull. No. 4 (2nd edition),
Swedish Nat. Sci. Res. Council, Stockholm, Sweden. 59 p.
Lb'froth, G. 1973. The mercury problem: a review at midway. Pages 63-
70 In: Trace substances in environmental health-VI. D. D. Hemphill
(EdTT, Univ. Missouri, Columbia.
Lovett, R. J., W. H. Gutenmann, I. S. Pakkala, W. D. Youngs, D. J. Lisk,
G. E. Burdick, and E. 0. Harris. 1972. A survey of the total
cadmium content of 406 fish from 49 New York state fresh waters.
J. Fish. Res. Board Can. 29(9): 1283-1290.
Lowman, F. G., T. R. Rice, and F. A. Richards. 1971. Accumulation and
redistribution of radionuclides by marine organisms. Pages 161-199
In; Radioactivity in the marine environment. National Academy of
Sciences, Washington, D.C.
Lucas, H. F., Jr., D. N. Edgington, and P. J. Colby. 1970. Concentrations
of trace elements in Great Lakes fishes. J. Fish. Res. Board Can.
27(4): 677-684.
•x.
Luoma, S. A., and E. A. Jenne. 1976. The availability of sediment-
bound cobalt, silver, and zinc to a deposit-feeding clam. Pages 1-
31 In: Proc. Symp. Biological Implications of Metals in the Environ-
ment, Sept. 29 to Oct. 1, 1975, Hanford, Washington.
87
-------
Maclnnes, J. R., F. P. Thurberg, R. A. Greig, and E. Gould. 19771 Long-
term cadmium stress in the cunner, Tautogoldbrus adspersus. Fish.-
Bull. 75(1): 199-203.
Marafante, E. 1976. Binding of mercury and zinc to cadmium-binding
protein in liver and kidney of goldfish (Carassius auratus L.).
Experientia 32(2): 149-150.
Marks, G. W. 1938. The copper content and copper tolerance of some
species of mollusks of the southern California coast. Biol. Bull. 75:
224-237.
Martin, D., and E. D. Goldberg. 1962. Uptake and assimilation of radio-
strontium by Pacific mackerel. Limnol. Oceanogr. 7(Supp.): Ixxvi-
Ixxxi.
Martin, J. H. 1970. The possible transport of trace metals via moulted
copepod exoskeletons. Limnol. Oceanogr. 15(5): 756-761.
Martin, 0. H., and W. W. Broenkow, 1975. Cadmium in plankton: Elevated
concentrations off Baja California. Science 190: 884-885.
Martin, 0. H., and A. R. Flegal. 1975. High copper concentrations in
squid livers in association with elevated levels of silver, cadmium,
and zinc. Mar. Biol. 30: 51-55.
Martin, M. H., Jr. 1971. Metals focus shifts to cadmium. Environ. Sci.
Technol. 5(9): 754-755.
Martin, M., M. D. Stephenson, and J. H. Martin. 1977. Copper toxicity
experiments in relation to abalone deaths observed in a power plant's
cooling waters. Calif. Fish Game 63(2): 95-100.
Mathis, B. 0., and T. F. Cummings. 1973. Selected metals in sediments,
water, and biota in the Illinois River. J. Water Pollut. Control Fed.
45(7): 1573-1583.
Mathis, B. J., and N. R. Kevern. 1975. Distribution of mercury, cadmium,
lead and thallium in a eutrophic lake. Hydrobiologia 46(2-3): 207-222.
Matsumura, F., Y. G. Doherty, K. Furukawa, and G. M. Boush. 1975. In-
corporation of 203Hg into methylmercury in fish liver: studies on
biochemical mechanisms"in vitro. Environ. Res. 10(2): 224-235.
Matsunaga, K. 1975. Concentration of mercury by three species of fish
from Japanese rivers. Nature 257(5521): 49-50.
Matthiessen, P., and A. E. Brafield. 1977. Uptake and loss of dissolved
zinc by the stickleback Gasierosteus aauleatus I. J. Fish Biol. 10:
399-410.
88
-------
McDermott, D. J., G. V. Alexander, D. R. Young, and A. J. Mearns. 1976.
Metal contamination of flatfish around a large submarine outfall. J.
Water Pollut. Control Fed. 48(8): 1913-1918.
McKee, J. E.f and H. W. Wolf. 1963. Water quality criteria. 2nd ed.
Publ. No. 3-A, State Water Quality Control Board, Sacramento,
California. 548 p.
McKim, J. M., and D. A. Benoit. 1974. Duration of toxicity tests for
establishing "no effect" concentrations for copper with brook trout
(Salvelinus fontinalis]. J. Fish. Res. Board Can. 31(4): 449-452.
McKim, J. M., G. K. Olson, G. W. Holcombe, and E. P. Hunt. 1976. Long-
term effects of methylmercuric chloride on three generations of brook
trout (Salvelinus fontinalis}: toxicity, accumulation, distribution,
and elimination. J. Fish. Res. Board Can. 33(12): 2726-2739.
Merlini, M., G. Pozzi, A. Brazzelli, and A. Berg. 1976. The transfer of
65Zn from natural and synthetic foods to a freshwater fish. Pages
226-229 ^TK Radioecology and energy resources. Ecol. Soc. Am.
Special Pub. No. 1.
Merlini, M., and G. Pozzi. 1977a. Lead and freshwater fishes: Part 1--
Lead accumulation and water pH. Environ. Pollut. 12: 168-172.
Merlini, M., and G. Pozzi. 1977b. Lead and freshwater fishes: Part 2—
Ionic lead accumulation. Environ. Pollut. 13: 119-126.
Miettinen, J. K. 1975. The accumulation and excretion of heavy metals
in organisms. Pages 155-166 In: Heavy metals in the aquatic environ-
ment, P. A. Krenkel (Ed.), Pergamon Press, Oxford.
Miettinen, J. K., T. Jaakkola, and M. Jarvinen.. 1975. Plutonium isotopes
in aquatic foodchains in the Baltic Sea. Pages 147-155 In: Impacts of
nuclear releases into the aquatic environment. International Atomic
Energy Agency, Vienna.
Mishima, J., and E. P. Odum, 1963. Excretion rate of Zn65 by Littorina
irrorata in relation to temperature and body size. Limnol. Oceanogr.
8(1): 39-44.
Morgan, F. 1964. The uptake of radioactivity by fish and shellfish. I.
13ltCaesium by whole animals. J. Mar. Biol. Assoc. U.K. 44: 259-271.
Morris, R. L., L. G. Johnson, and D. W. Ebert. 1972. Pesticides and
heavy metals in the aquatic environment. Health Lab. Sci. 9(2):
145-151.
Mount, D. I. 1964. An autopsy technique for zinc-caused fish mortality.
Trans. Am. Fish. Soc. 93(2): 174-182.
89
-------
Mount, D. I. 1966. The effect of total hardness and pH on acute toxicity
of zinc to fish. Air Water Pollut. Int. J, 10: 49-56.
Mount, D, I., and C. E. Stephen. 1967. A method for detecting cadmium
poisoning in fish. J. Wild!. Manage. 31(1): 168-172.
Nakatani, R. E., and R. F. Foster. 1963. Effect of chronic feeding of
Sr90_y90 on rainbow trout. Pages 359-362 In_: Radioecology. V.
Schultz and A. W. Klement, Jr. (Eds.)s Reinhold Pub!. Corp., New
York.
National Academy of Sciences, National Academy of Engineering. 1973.
Water quality criteria 1972. EPA Ecol. Res. Ser. EPA-R3-73-033, U.S.
Environmental Protection Agency, Washington, D.C. 594 p.
Nehring, R. EL 1976. Aquatic insects as biological monitors of heavy
metal pollution. Bull. Environ. Contam. Toxicol. 15(2): 147-154.
Neville, G. A.s and M. Berlin. 1974. Identification and biotransformation
of organomercurial compounds in living systems. A review of current
understanding. Environ. Res. 7: 75-82.
Noel-Lambot, F. 1976. Distribution of cadmium, zinc and copper in the
mussel Mytilus edulis. Existence of cadmium-binding proteins similar
to metallothioneins. Experientia 32: 324-325.
Norstrom, R. J., A. E. McKinnon, and A. S. W. deFreitas. 1976. A
bioenergetic-based model for pollutant accumulation by fish. Simula-
tion of PCB and methylmercury residue levels in Ottawa River yellow
perch (Peroa flavescens). J. Fish. Res. Board Can. 33(2): 248-267.
Noshkin, V. E. 1972. Ecological aspects of plutonium dissemination in
aquatic environments. Health Phys. 22(6).: 537-549.
Nuorteva, P., and E. Hasanen. 1975. Bioaccumulation of mercury in
Myoxooephalus quadrieornis (L.) (Teleostei, Cottidae) in an unpolluted
area of the Baltic. Ann. Zool. Fennici 12: 247-254.
O'Hara, J. 1973. Cadmium uptake by fiddler crabs exposed to temperature
and salinity stress, J. Fish. Res. Board Can. 30(6): 846-848.
Olson, 6. F., D. I. Mount, V. M. Snarski, and T. W. Thorslund. 1975.
Mercury residues in fathead minnows, Pimephales promelas Rafinesque,
chronically exposed to methylmercury in water. Bull. Environ. Contam.
Toxicol. 14(2): 129-134.
Olsson, M. 1976. Mercury level as a function of size and age in northern
pike, one and five years after the mercury ban in Sweden. Ambio 5(2):
73-76.
90
-------
Ophel, I. L., and J. M. Judd. 1967. Experimental studies of radiostrontium
accumulation by freshwater fish from food and water. Pages 859-865 In_:
Radioecological processes. B. Aberg and F. P. Hungate (Eds.), Pergamon
Press, London.
Osterberg, C. 1962. Zn65 content of salps and euphausiids. Limnol.
Oceanogr. 7(4): 478-479.
Pagenkopf, G. K., and D. R. Neuman. 1974. Lead concentrations in native
trout. Bull. Environ. Contam. Toxicol. 12(1): 70-75.
Pakkala, I. S., W. H. Gutenmann, D. J. Lisk, G. E. Burdick, and E. J.
Harris. 1972. A survey of the selenium content of fish from 49 New
York state waters. Pestic. Monit. J. 6(2): 107-114.
Pakkala, I. S., M. N. White, G. E. Burdick, E. J. Harris, and D. J. Lisk.
1972. A survey of the lead content of fish from 49 New York state
waters. Pestic. Monit. J. 5(4): 348-355.
Pakkala, I. S., M. N. Uhite, D. J. Lisk, G. E. Burdick, and E. J. Harris.
1972. Arsenic content of fish from New York state waters. N.Y. Fish
Game J. 19(1): 12-31.
Panel on Nickel. 1975. Nickel. Committee on Medical and Biologic Effects
of Environmental Pollutants, National Research Council, National
Academy of Sciences, Washington, D.C. 277 p.
Papadopoulou, C., G. D. Kanias, and E. Moraitopoulou-Kassimati. 1976.
Stable elements of radioecological importance in certain echinoderm
species. Mar. Pollut. Bull. 7(8): 143-144.
Pascoe, D., and D. L. Mattey. 1977. Studies on the toxicity of cadmium
to the three-spined stickleback Gasterosteus aauleatus L. J. Fish
Biol. 11(2): 207-215.
Patrick, F. M., and M. Loutit. 1976. Passage of metals in effluents,
through bacteria to higher organisms. Water Res. 10(4): 333-335.
Patterson, C., and D. Settle. 1977. Comparative distributions of alka-
lies, alkaline earths and lead among major tissues of the tuna
Thunnua alalunga. Mar. Biol. 39: 289-295.
Pendleton, R. C. 1-959. Effects of some environmental factors on bio-
accumulation of cesium-137 in an aquatic community. Pages 42-46 In:
Hanford Biology Research Annual Report for 1958. J. J. Davis (EdTJ,
HW-59500, Hanford Atomic Products Operation, Richland, Washington.
Pentreath, R. J. 1973. The accumulation and retention of 65Zn and 54Mn by
the plaice, Pleuroneotes platessa L. J. Exp. Mar. Biol. Ecol. 12:
1-18.
91
-------
Peterson, C. L., W. L. Klawe, and G. D. Sharp. 1973. Mercury in tunas:
a review. Fish. Bull. 71(3): 603-613.
Piavaux, A. 1977. (.'influence du cadmium sur Tactivite de la phosphatase
alcaline dans divers tissus de Lepomis gibbosus L. (Pisces;
centrarchidae). Hydrobiologia 55(3)": 251-256. [In French with
English abstract and summary.]
Pickering, Q. H. 1974. Chronic toxicity of nickel to the fathead minnow.
J. Water Pollut. Control Fed. 46(4): 760-765.
Pickering, Q. H., and C. Henderson. 1966. The acute toxicity of some
heavy metals to different species of warmwater fishes. Air Water
Pollut. Int. J. 10: 453-463.
Pilkey, 0. H., and H. G. Goodell. 1963. Trace elements in recent mollusk
shells. Limnol. Oceanogr. 8(2): 137-148.
Potter, L., D. Kidd, and D. Standiford.- 1975. Mercury levels in Lake
Powell. Bioamplification of mercury in man-made desert reservoir.
Environ. Sci. Technol. 9(1): 41-46.
Preston, A. 1973. Cadmium in the marine environment of the United
Kingdom. Mar. Pollut, Bull. 4: 105-107.
Preston, A., D. F. Jefferies, and J. W. R. Dutton. 1967. The concen-
trations of caesium-137 and.strontium-90 in the flesh of brown trout
taken from rivers and lakes in the British Isles between 1961 and
1966: the variables determining the concentrations and their use
in radiological assessments. Water Res. 1(7): 475-496.
Pringle, B. H., D. E. Hissong, E. L. Katz, and S. T. Mulawka. 1968.
Trace metal accumulation by estuarine mollusks. J. Sanit. Eng.
Div., Am. Soc. Civ. Eng. 94: 455-475.
Ramamoorthy, S., S. Springthorpe, and D. J. Kushner. 1977. Competition
for mercury between river sediment and bacteria. Bull. Environ.
Contam. Toxicol. 17(5): 505-511.
Raymont, J. E. G., and J. Shields. 1963. Toxicity of copper and chromium
in the marine environment. Int. J. Air Water Pollut. 7: 435-443.
Rehwoldt, R., D. Karimian-Teherani, and H. Altmann. 1975. Measurement
and distribution of various heavy metals in the Danube River and
Danube Canal aquatic communities in the vicinity of Vienna, Austria.
Sci. Total Environ. 3: 341-348.
Rehwoldt, R., and D. Karimian-Teherani. 1976. Uptake and effect of
cadmium on zebrafish. Bull. Environ. Contam. Toxicol. 15(4): 442-446.
92
-------
Rehwoldt, R., D. Karimian-Teherani, and H. Altmann. 1976. Distribution
of selected metals in tissue samples of carp, Cyprinus carpio. Bull.
Environ. Contain. Toxicol. 15(3): 374-377.
Reimold, R. 0., and M. H. Shealy, Jr. 1976. Chlorinated hydrocarbon
pesticides and mercury in coastal young-of-the-year finfish, South
Carolina and Georgia—1972-74. Pestic. Monit. J. 9(4): 170-175.
Renfro, W. C., S. W. Fowler, M. Heyraud, and J. La Rosa. 1975. Relative
importance of food and water in long-term zinc65 accumulation by
marine biota. J. Fish. Res. Board Can. 32(8): 1339-1345.
Renzoni, A., and E. Bacci. 1976. Bodily distribution, accumulation and
excretion of mercury in a fresh-water mussel. Bull. Environ. Contam.
Toxicol. 15(3): 366-373.
Richins, R. T., and A. C. Risser, Jr. 1975. Total mercury in water,
sediment, and selected aquatic organisms, Carson River, Nevada—1972.
Pestic. Monit. J. 9(1): 44-54.
Robertson, T., G. D. Waugh, and J. C. M. Mol. 1975. Mercury levels in New
Zealand snapper Chrysopkrys auratus. N.Z. J, Mar. Freshwater Res.
9(3): 265-272.
Romeril, M. G., and M. H. Davis. 1976. Trace metal levels in eels grown
in power station cooling water. Aquaculture 8: 139-149.
Rosenthal, H. L. 1963. Uptake, turnover and transport of bone seeking
elements in fishes. Ann. N.Y. Acad. Sci. 109(1): 278-293.
Rossi, L. C., G. G. Mastinu, G. F. Clemente, and G. P. Santaroni. 1976.
Contenuto di mercuric ed altri elementi in campioni di tonno in
scatola. (Content of mercury and other elements in samples of canned
tunafish.) Riv. Sci. Teen. Alim. Nutr. Urn. 6(2): 97-100. [In
Italian with English summary.]
Roth, I., and H. Hornung. 1977. Heavy metal concentrations in water,
sediments, and fish from Mediterranean coastal area, Israel.
Environ. Sci. Technol. 11(3): 265-269.
Rowe, D. W., and E. J. Massaro. 1974. Cadmium uptake and time dependent
alterations in tissue levels in the white catfish Ictalurus oatus
(Pisces: Ictaluridae). Bull. Environ. Contam. Toxicol. 11(3): 244-
249.
Ruohtula, M., and J. K. Miettinen. 1975. Retention and excretion of
203Hg-labelled methylmercury in rainbow trout. Oikos 26: 385-390.
Sana, J. G. 1972. Significance of mercury in the environment. Residue
Rev. 42: 103-163.
93
-------
Sandholm, M., H. E. Qksanen, and L. Pesonen. 1973, Uptake of selenium
by aquatic organisms. Limnol. Oceanogr. 18(3): 496-499.
Sandhu, S. S. 1977. Study on the post-mortem identification of pollu-
tants in the fish killed by water pollution: detection of arsenic.
Bull. Environ. Contam. Toxicol. 17(3): 373-378.
Schell, W. R., and R. L. Watters. 1975. Plutonium in aqueous systems.
Health Phys. 29: 589-597.
Scherer, E., F. A. J. Armstrong, and S. H. Nowak. 1975. Effects of
mercury-contaminated diet upon walleyes, Stizostedion vitrewn
vitreum (Mitchill). Fish. Mar. Serv. Res. Dev. Tech. Rep. No. 597.
21 p.
Schiffman, R. H. 1959. The uptake of strontium from diet and water by
rainbow trout. Pages 16-19 In: Hanford Biology Research Annual
Report for 1958. J. J. Davis (Ed.), HW-59500, Hanford Atomic Products
Operation, Richland, Washington.
Schiffman, R. H. 1961a. A perfusion study of the movement of strontium
across the gills of rainbow trout (Salm
-------
Shealy, M. H., Jr., and C. A. Carlson. 1973. Accumulation and retention
of strontium-85 marks by young largemouth bass. Pages 307-317 In:
Proc. 3rd National Symposium on Radioecology. D. Nelson (Ed.),
USAEC CONF-710501, Springfield, Virginia.
Shin, E.-B., and P. A. Krenkel. 1976. Mercury uptake by fish and bio-
methylation mechanisms. J. Water Pollut. Control Fed. 48(3):
473-501.
Shukla, S. S., and H. V. Leland. 1973. Heavy metals: A review of lead.
J. Water Pollut. Control Fed. 45(6): 1319-1331.
Shultz, C. D., D. Crear, J. E. Pearson, J. B. Rivers, and J. W. Hylin.
1976. Total and organic mercury in the Pacific blue marlin. Bull.
Environ. Contam. Toxicol. 15(2): 230-234.
Shuster, C. N., Jr., and B. H. Pringle. 1969. Trace metal accumulation by
the American eastern oyster, Crassostrea virginica. Proc. Nat.
Shellfish. Assoc. 59: 91-103.
Sinley, J. R., J. P. Goettl, Jr., and P. H. Davies. 1974. The effects of
zinc on rainbow trout (Salmo gaivdnevi] in hard and soft water. Bull.
Environ. Contam. Toxicol. 12(2): 193-201.
Skerfving, S. 1972. Mercury in fish--some toxicological considerations.
Food Cosmet. Toxicol. 10: 545-556.
Slater, J. V. 1961. Comparative accumulation of radioactive zinc in
young rainbow, cutthroat and brook trout. Copeia 1961(2): 158-161.
Slonim, A. R. 1973. Acute toxicity of beryllium sulfate to the common
guppy. J. Water Pollut. Control Fed. 45(10): 2110-2121.
Smith, A. L., R. H. Green, and A. Lutz. 1975. Uptake of mercury by
freshwater clams (family Unionidae). J. Fish. Res. Board Can.
32(8): 1297-1303.
Smith, T. G., and F. A. J. Armstrong. 1975. Mercury in seals, terrestrial
carnivores, and principal food items of the Inuit, from Holman,
N. W. T. J. Fish. Res. Board Can. 32(6): 795-801.
Solbe, J. F. de L. G., and V. A. Flook. 1975. Studies on the,toxicity of
zinc sulfate and of cadmium sulfate to stone loach Noemaeheilus
barbatulus (L.) in hard water. J. Fish Biol. 7: 631-637.
Solbe, J. F. de L. G., and V. A. Cooper. 1976. Studies on the toxicity
of copper sulfate to stone loach Noemacheilus barbatulus (L.) in
hard water. Water Res. 10(6): 523-527.
Sorensen, E. M. B. 1976a. Thermal effects on the accumulation of arsenic
in green sunfish, Lepomis eyanellus. Arch. Environ. Contam. Toxicol.
4: 8-17.
95
-------
Sorensen, E. M. B. 1976b. Toxicity and accumulation of arsenic in green
sunfish, Lepomis cyanellus, exposed to arsenate in water. Bull.
Environ. Contam. Toxtcol. 15(6): 756-761.
Sorenson, J. R. J., I. R. Campbell, L. B. Tepper, and R. D. Lingg. 1974.
Aluminum in the environment, and human health. Environ. Health Per-
spectives 8: 3-95.
Spangler, W. J., J. L. Spigarelli, J. M. Rose, and H. M. Miller. 1973.
Methylmercury: bacterial degradation in lake sediments. Science
180: 192-193.
Spehar, R. L. 1976. Cadmium and zinc toxicity to flagfish, Jordanella
floridae. J. Fish. Res. Board Can. 33(9): 1939-1945.
Sprague, J. B. 1964. Lethal concentrations of copper and zinc for young
Atlantic salmon. J. Fish. Res. Board Can. 21(1): 17-26.
Stapleton, R. P. 1968. Trace element$ in.tissues of the calico bass
Paralabrax clathratus (Girard). Bull. South. Calif. Acad. Sci. 67(1):
49-58.
* f>
Steinnes, E., T. HSstein, G. Norheim, and A. Fr0slie. 1976. Mercury in
various tissues of fish caught downstream of a wood pulp factory in
the Kammerfoss River, South Norway. Nord'. Veterinaermed. 28: 557-563.
Stewart, J., and M. Schulz-Baldes. 1976. Long-term lead accumulation in
abalone (Haliotis spp.) fed on lead-treated brown algae (Egregia
laevigata). Mar. Biol. 36: 19-24.
Stopford, W., and L. J. Goldwater. 1975. Methylmercury in the environment:
a review of current understanding. Environ. Health Perspect. 12: 115-
118.
Study Group on Mercury Hazards. 1971. Hazards of mercury. Environ. Res.
4(1): 1-69.
Stumm, W., and J. J. Morgan. 1970. Aquatic chemistry. Wiley-Interscience,
New York. 583 p.
Suzuki, T., and M. Hatanaka. 1974. Experimental investigation on the
biological concentration of mercury—I.. On the rate of mercury transfer?
through the food chain from jack mackerel to young yellowtail. Bull.
Jpn. Soc. Sci. Fish. 40(11): 1173-1178. [In Japanese with English
summary.]
Suzuki, T., T. Takemoto, H. Kashi'wazaki, M. Togo, H. Toyokawa, and T.
Miyama. 1976. Man, fish, and mercury on small islands in Japan.
Tohoku J. Exp. Med. 118: 181-198.
Talbot, V. W., R. J. Magee, and M. Hussain. 1976. Cadmium in Port Phillip
Bay mussels. Mar. Pollut. Bull. 7(5): 84-86.
96
-------
Tarzwell, C. M., and C. Henderson. 1960. Toxicity of less common metals
to fishes. Ind. Wastes 5: 12.
Terhaar, C. 0., W. S. Ewell, S. P. Dziuba, W. W. White, and P. J. Murphy.
1977. A laboratory model for evaluating the behavior of heavy metals
in an aquatic environment. Water Res. 11(1): 101-110.
Thomas, N. A. 1975. Accumulation and transport of energy related pollu-
tants by benthos. 2nd ICMSE conference, March 25-27, 1975. 12 p.
Thompson, J. A. J., J. C. Davis, and R. E. Drew. 1976. Toxicity, uptake
and survey studies of boron in the marine environment. Water Res.
10(10): 869-875.
Thurberg, F. P., A. Calabrese, and M. A. Dawson. 1974. Effects of silver
on oxygen consumption of bivalves at various salinities. Pages 67-78
In: Pollution and physiology of marine organisms. Academic Press,
New York.
Tong, S. S. C., W. D. Youngs, W. H. Gutenmann, and D. J. Lisk. 1974. Trace
metals in Lake Cayuga lake trout (SalveUnus namaycush) in relation to
age. 0. Fish. Res. Board Can. 31(2): 238-239.
Trollope, D. R., and B. Evans. 1976. Concentrations of copper, iron, lead,
nickel and zinc in freshwater algal blooms. Environ. Pollut. 11: 109-
116.
Tsai, S.-C., G. M. Boush, and F. Matsumura. 1975. Importance of water pH
in accumulation of inorganic mercury in fish. Bull. Environ. Contam.
Toxicol. 13(2): 188-193.
Ullmann, W. W., R. W. Schaefer, and W. W. Sanderson. 1961. Arsenic accumu-
lation by fish in lakes treated with sodium arsenite. J. Water Pollut.
Control Fed. 33(4): 416-418.
Uthe, J. F., F, M. Atton, and L. M. Royer. 1973. Uptake of mercury by caged
rainbow trout (Salmo gairdneri) in the South Saskatchewan River. J.
Fish. Res. Board Can. 30(5): 643-650.
Uthe, 0. F., and E. G. Bligh. 1971. Preliminary survey of heavy metal
contamination of Canadian freshwater fish. J. Fish. Res. Board Can.
28(5): 786-788.
Uthe, J. F., and J. Reinke. 1975. Arsenate ion reduction in non-living
biological materials. Environ. Lett. 10(2): 83-88.
van Weers, A. W. 1975. The effect of temperature on the uptake and reten-
tion of 60Co and 65Zn by the common shrimp Crangon crangon (L.) Pages
35-49 In_: Combined effects of radioactive, chemical and thermal
releases into the environment. International Atomic Energy Agency,
Vienna.
97
-------
Varanasi, U., and D. Markey. 1977. Effect of calcium on retention of lead
in fish skin. Fed. Proc. Fed. Am. Soc. Exp. Biol. 36(3): 772.
Voors, A. W., and M. S. Shuman. 1977. Liver cadmium levels in North
Carolina residents who died of heart disease. Bull. Environ. Contam.
Toxicol. 17(6): 692-696.
Ward, E. E. 1966. Uptake of plutonium by the lobster Homarus vulgaris.
Nature 209(5023): 625-626.
Ward, J. V. 1973. Molybdenum concentrations in tissues of rainbow trout
(Salmo gairdneri] and kokanee salmon (Oncorhynahus nevkx) from waters
differing widely in molybdenum content. J. Fish. Res. Board Can.
30(6): 841-842.
Watling, H. R., and R. J. Watling. 1976a. Trace metals in oysters from
Knysna estuary. Mar. Pollut. Bull. 7(3): 45-48.
Watling, H. R., and R. J. Watling. 1976b. Trace metals in Choromytilus
meridionalis. Mar. Pollut. Bull. 7(5): 91-94.
Weast, R. C. (Ed.). 1975. Handbook of chemistry and physics. 56th ed. •
CRC Press, Cleveland, Ohio.
Wedemeyer, G. 1968. Uptake and distribution of Zn65 in the coho salmon
egg (Oneorhynchus kisutoh). Comp. Biochem. Physio!. 26: 271-279.
Westermark, T., T. Odsjo, and A. G. Johnels. 1975. Mercury content of
bird feathers before and after Swedish ban on alkyl mercury in
agriculture. Ambio 4(2): 87-92.
Westb'6, G. 1973. Methylmercury as percentage of total mercury in flesh
and viscera of salmon and sea trout of various ages. Science 181:
567-568.
Wharfe, 0. R.j and W. L. F. Van Den Broek. 1977. Heavy metals in macro-
invertebrates and fish from the lower Medway estuary, Kent. Mar.
Pollut. Bull. 8(2): 31-34.
Wiebe, A. H., E. G. Gross, and D. H. Slaughter. 1931. The arsenic content
of large-mouth black bass (Mieropterus salmoides lacepede] fingerlings.
Trans. Am. Fish. Soc. 61: 150-163.
Wilber, C. G. 1969. The biological aspects of water pollution. Charles
C. Thomas Pub., Springfield, Illinois. 296 p.
Williams, L. G., and Q. Pickering. 1961. Direct and food-chain uptake of
cesium137 and strontium85 in bluegill fingerlings. Ecology 42(1):
205-206.
98
-------
Williams, R. J., N. J. Mackay, L. C. Collett, and J. L. Kacprzak. 1976.
Total mercury concentration in some fish and shellfish from New South
Wales estuaries. Food Technol. Aust. 28(1): 8-10.
Willis, J. N., and N. Y. Jones. 1977. The use of uniform labeling with
zinc-65 to measure stable zinc turnover in the mosquito fish, Gambusia
affinis—I. Retention. Health Phys. 32: 381-387.
Windom, H., R. Stickney, R. Smith, D. White, and F. Taylor. 1973. Arsenic,
cadmium, copper, mercury, and zinc in some species of North Atlantic
finfish. J. Fish. Res. Board Can. 30(2): 275-279.
Wisconsin Department of Natural Resources. 1974. Concentration of metals
in fish. Tech. Bull. No. 74, Dep. Natural Resources, Madison, Wisconsin,
p. 8-15.
Wobeser, G. 1975. Prolonged oral administration of methylmercury chloride
to rainbow trout (Salmo gaivdneri] fingerlings. 0. Fish. Res. Board
Can. 32(11): 2015-2023.
Wobeser, G., N. 0. Nielsen, and B. Schiefer. 1976. Mercury and mink. I.
The use of mercury contaminated fish as a food for ranch mink. Can.
0. Comp. Med. 40(1): 30-33.
Wojtalik, T. A. 1971. Accumulation of mercury and its compounds. J.
Water Pollut. Control Fed. 43(6): 1280-1292.
Wolfe, D. A. 1970. Levels of stable Zn and 65Zn in Crassostrea virginioa
from North Carolina. J. Fish. Res. Board Can. 27(1): 47-57.
Wood, J. M., F. S. Kennedy, and C. G. Rosen. 1968. Synthesis of methyl-
mercury compounds by extracts of a methanogenic bacterium. Nature
220(5163): 173-174.
Wood.'O. M. 1974. Biological cycles for toxic elements in the environ-
ment. Science 183: 1049-1052.
Wright, D. A. 1976. Heavy metals in animals from the north east coast.
Mar. Pollut. Bull. 7(2): 36-38.
Wright, D. A. 1977a. The effect of salinity on cadmium uptake by the
"tissues of the shore crab Carcinus maenas. 0. Exp. Biol. 67: 137-146.
Wright, D. A. 1977b. The uptake of cadmium into the haemolymph of the
shore crab Carcinus maenas: the relationship with copper and other
divalent cations. J. Exp. Biol. 67: 147-161.
Wright, D. A. 1977c. The effect of calcium on cadmium uptake by the
shore crab Carcinus maenas. 0. Exp. Biol. 67: 163-173.
Yamamoto, T., T. Tamaoka, T. Fujita, and C. Isoda. 1973. Boron content
in marine plankton. Rec. Oceanogr. Works Jpn. 12(1): 13-21.
99
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Yamanaka, S., and K. Ueda. 19_75. tHigh ethylmercury jn river fish by*
man-made pollution. Bull. Environ. Contam. Toxicol. '14"(4yi 409-414*.
Zaroogian, G. E., and S. Cheer.. 1976. Accumulation of cadmium by the
American oyster, Crassostrea virginiaa. Nature 261: 408-410.
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APPENDIX
Index to the scientific and common names of organisms referred to in the
text. Nomenclature is that used by the original author(s).
FISHES
Scientific Names
Acanthopagrus sp. 46
Alburnus sp. 29
Alosa aestivalis 29
Alosa pseudoharengus 68
Amia. calva 42
Ambloplites rupestz»is 39
Anahoa mitohilli 71
Anguilla anguilla 49
Anoplopoma firribria 45
Antimora rostrata 27, 34, 72
Bairdiella ohpysux>a 45
Belone belone 15, 16
Brachydanio rev-io 14
Brevoovtia tyrarmus 71
Brosme brosme 45
Carassius auratus 13, 23, 56, 58, 61, 62
Caraseius carassiue 44
Catostorrus latipinnis 42
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FISHES (continued)
Chasmichthys gulosus 65
Chrysophrys auratus 45
Clarias lazera 20, 24
Clupea harengus 15, 16
CoTegonus elupeaformis 34
Coregonus lavaretus 24
Covydoras punotatus 14
Cyprinus carpio 29, 41, 42, 63, 71
Engraulis japoniaa 41
Esoa: luciws 24, 34, 40, 42, 43, 44
Esox niger 29
Euthynnus alletteratus 21
Fundulus heterocl-itus 16, 27, 65, 66
Gadus morhua 64
Gambusia affinis 37, 38, 60
Gasterosteus aculeatus 14, 61
Girella tricuepidata 46
Gobius 63
Eelieolenus dactylopterus 45
Hippoglossus stenolepis 45
Hypotremata sp. 44
JctaZwrue oatus 13
latalurus nebulosus 26, 60
lataliams punotatus 42, 51
Jordanella floridae 62
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FISHES (continued)
Katsuwonus pelamis 30
Labidesthes s-ioaulus 29
Lagodon rhomboides 71
Lebistes 59
Lebistes reticulatus 14
Leiostomus xanfhurus 71
Lepomis cyanellue 9, 10
Lepomis gibbosus 15, 20, 30, 31, 63
Lepomis macyochivus 8, 14, 15, 26, 29, 56, 63
Makaiva. nigricans 46
Micropogon undulatus 21, 45, 65, 71
Micropterus dolomieui, 42, 68
Mioropterus salmoides 9, 15, 42, 56, 59
Microstomus pacificus 7
Molva molva 44
Morone chrysops 68
Myoxocephalus quadricornis 45
Neothunnus maaropterus 7, 30
Noemaaheilus bapbatulus 13, 27
Notropis atherinoides 38
Notropis hudsonius 68
Oblata melam&a 44
Oncorhynchus kisutoh 62
OnoorhynaJms nerka 12, 48
Onoorhynchus tshawytsoha 61
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FISHES (continued)
Oryzias latipes 39 ;
Paraldbvax clatfoatus 7, 25, 29, 34, 69
* • .
Paraliehthys dentatus 2-1"
Perca flavesoens 39, 41, 68
Peroa fluviatilis 24, 71
Pereopsis omiseomaycus 68
Pimephales pvamelas 38, 39, 41, 47, 57
Platichthys flesus 15, 16,^45 _ .,
Pleuronectes platessa 21°; 34, 50', 52, 65
Pneumatoplioyus diego 59 . ., -_
Poeoi'i'ia retiaulata 11, 37, 38
Pomatomus saltatrix 21, 27, 34, 72
Pomoxis n-i-gvamaculatus 9, 42
Pseudopleuroneates americanus 15, 39
Raja clavata 21
Rooaus chrysops 42
l?udariue eroodes 65
Salmo alarki 56, 61
5aZroo gairdneri 8, 15, 22, 26, 30, 38, 39, 40, 43, 47, 48, 58, 59,' 61
Salmo salar 34, 60, 70
Salmo trutta 21, 34, 43, 70, 71
Salvelinus alpinus 40
Salvelinus fontinalis 14, 26, 31, 39, 47, 61
Salvelinus namycush 7, 22, 25V 29, 31, 34, 48, 68
Sebastes marinus 44
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FISHES (continued)
Semotilus atramaculatus 54
Seriora quinqueradiata 41
Squalus acanthlas 45
Stizostedion vitreum vitreum 40, 41, 42
Tautogolabrus adspersus 16
Thunnus alalunga 30, 72
Thunnus obesus 44
Thunnus ttynnus 44
Thymallus thymallus 43
Umbrina civrhosa 44, 45
Xiphias gladius 44
Common Names
albacore--see Thunnus alalunga
alewife—see Alosa pseudoharengue
anchovy—see Engraulis japonioa
arctic char—see Salvelinus alpinus
Atlantic cod--see Gadus morhua
Atlantic croaker—see Miavopogon undulatus
Atlantic menhaden—see Brevoortia tyrannus
Atlantic salmon--see Salmo salar
bay anchovy—see Anohoa mitohilli
bigeye tuna—see Thunnus obeaus
blackbellied redfish—see Helicolenus daatylopterus
black crappie—see Pomoxie n-igromaaulatus
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FISHES (continued)
blackfish—see Girella triouspidata
blueback herring—see Alosa aestivalis
bluefin tuna--see Thunnus thynnus
bluefish—see Pomatomus saltatpix
bluegill—see Lepomis maerochirus
blue marl in—see Makaiva nigpioans
bream—see Acanthopagrus sp.
brook silverside—see Labidesfhes sicoulus
brook trout—see Salvelinus fontinalis
brown bullhead—see letalurus nebulosus
brown trout—see Salmo trutta
calico bass—see Paralabrax clatfoatus and Pomoxis nigromaaulatus
carp—see Cyprinus Qarpio
catfish—see Corydovas punctatus
chain pickerel—see Esox niger
channel catfish—see Ictalurus punotatus
Chinook salmon—see Oncorhynckus tshauytscfaz
coho salmon—see Oncorhynchus kisutah
creek chub—see Semotilus atromaculatus
crucian carp—see Carassius earassius
cunner—see Tautogolabrus adspersus
cusk—see Bvosme brosme
cutthroat trout—see Salmo elarki
dover sole—see Miarostomus pacificus
emerald shiner—see Notropis atherinoides
106
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FISHES (continued)
European eel--see Anguilla anguilla
fathead minnow—see Pimephales pramelas
filefish—see Rudarius ercodes
flagfish--see Jordanella floridae
flannelmouth sucker—see Catostorms latipinnis
fourhorn sculpin—see Myoxocephalus quadricornis
garpike—see Belone belone
goldfish—see Carassius-aicpatus
grayling—see Thymallus ttymallus
green sunfish—see Lepomis oyanellus .
guppy—see Poecilia reticulata, Lebistes, and Lebistes retioulatus
halibut—see Hippoglossus stenolepis
herring—see Clupea harengus
Japanese medaka—see Oryzias latipes
lake trout—see Salveli-nus namaycush
lake whitefish—see Coregonus olupeaformis
largemouth bass—see Micropterus sahnoides
ling--see Molva molva
little tuna—see Euthynnus alletteratus
marine goby—see Chasmichthys gulosus
morid—see Antimora vostrata
mosquitofish—see Gambusia affinis
mudfish—see Amia calva
mummichog—see Fundulus heteroclitus
Nile catfish—see Clarias lazera
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FISHES (continued)
northern pike—see Esox luoius
Pacific mackerel—see Pneumatophorus diego'
Pacific sablefish—see Anoplopoma fimbria ~
perch—see Perca fluviatilis
pike—see Esox lueius
pinfish—see Lagodon rhomboides
plaice—see Pleuronectes platessa
pumpkinseed sunfish—see Lepomis gibbosus
rainbow trout—see Salmo gairdneri'
red-fish—see Sebastes,,maz>inus , . ,
... -«•*•. .<• ;.»'
rock bass—see AmblopHtes rupestris
silver perch—see Bairdiella chrysura
skipjack—see Katsuwonus pelamie
smallmouth bass—see Micropterus dolomieui
snapper—see Chpysophrys aweatus
sockeye salmon—see Oneorhynehus nerka
spiny dogfish—see Squalus acanthias
spot—see Leiostomus xanthurus
spottail shiner—see Notropis hudsonius
stone loach—see Noemaoheilus bcwbatulus
three-spined stickleback—see Gasterosteus asuleatus
summer flounder—see ParaHohthys dentatus
thornback ray—see Raja alavata
trout-perch—see Percopsis omiscomaycus
walleye—see Stisostedion vitreum vitreum
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FISHES (continued)
white bass—see Morons chrysops
white catfish—see Ictalurus oatus
whitefish--see Coregonus lavaretus
winter flounder—see Pseudopleuroneotes ameriaanus
yellow perch—see Perea flavescens
yellowfin tuna—see Neothunnus macropterus
yellowtail—see Seriora quinqueradiata
zebrafish—see Braahydanio rerio
INVERTEBRATES
Scientific Names
Ampullaria paludosa 14
Anodonta grandis 38
Artemia sa1i.no. 63
Aquipeeten irradians 16, 64
Asellus meridianus 27, 31
Aetaaus sp. 53
Austropotcanobius pallipes pallipes 63
Cambarus bartoni bartoni 52
Cambarus longulus longerostris 58
Cambarus robustus 52
Cambarus rusticus 52
Cancer magister 9, 10
Cancer pagurus 50
Canaer productus 53
109
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INVERTEBRATES (continued)
Carcinus maenas 17, 24, 63*
Choromytilus meridional-is 73
Crangon crangon 25, 65
Crassostrea commercial-is 46
Crassostrea gigas 12, 25, 64, 73
Crassostrea margaritaeea 73
Crassostrea virginica 16, 17, 23, 25, 28, 29, 32, 34, 49, 64, 65
Daphnia magna 41, 56
Ensis ensis 29
Ensia sp. 25
Ephemerella grandis 27
Euphausia pacifica 64
Gammarus zaddachi 32
Haliotis craoherodii 28
Haliotis ruber 46
Haliotis rufescens 18, 28, 32, 57
Harmothoe sarsi 32
Helix aspersa 27
Hermione hystrix 23
Eomarus americanus 16, 17
Homarus vulgaris 51, 64
Lampsilis siliquoidea rosacea 70
Ligumia sp. 56
Littorina irrorata 65
Littorina littorea 35, 70, 71
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INVERTEBRATES (continued)
Loligo opalescens 27
Lysmata setioaudata 17, 51, 55, 63
Maooma balthiaa 73
Margaritifera sp. 56, 57
Meganyctiphanes norvegiea 55
Meroenaria mercenaria 64
Meretrix meretrix lusoria 52
Mesidotae entonom 32
Mulinia lateral-is 17
Mya arenayia 17
Mytilus californianus 27, 32, 46
Mytilus edulis 14, 17, 27, 32, 49, 52, 65
Mytilus galloprovineialis 17, 51, 55
Mytilus sp. 25, 32
Nereis 65
Nereis virens 23, 28
Nucula proxima 17
Ommastrephes bartrami 27
Orconectes obsourus 52
Oraoneotes rustiaus rustiaus 52
Ostrea edulis 73
Peaten irradians 64
Polypus bimaaulatus 27
Pseudanodonta ccmplanata 38
Pteronaroella badia 13
111
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INVERTEBRATES (continued)
Pteronavays californica 13, 27
Salpa sp. 64
Scrobicularia piano. 24
Strongylocentrotus pulaherrimus 65
Sympleototeuthis oualaniensis 27
Tapes japoniea 65
Thais lapillus 35, 70, 71
Tubifex sp. 27, 35, 69, 70
Uea pugilatoT 17
Unio cfv. elongatulus 43
Venus meraenaria 64
Viviparus ater 63
Common Names
American lobster—see Homarus americanus
American eastern oyster—see Crassostrea virginiaa
American oyster—see Cvassostrea virginica
bay scallop—see Pec ten irradians and Aquipeoten irradians
benthic shrimp—see Lysmata set-icaudata
black abalone—see Ealiotis craoherodii
blacklip abalone—see Ealiotis ruber
common Mediterranean mussel—see Mytilus galloprovincialis
common shrimp—see Crangon arangon
common terrestrial snail--see Helix aspersa
dungeness crab—see Cancer magister
112
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INVERTEBRATES (continued)
fiddler crab--see Uca pugilator
hard-shell clam—see Venus meraenaria
infusoria snail—see Ampullaria paludosa
Pacific oyster—see Crassostrea gigas
red abalone--see Ealiotis rufesoens
sea mussel--see Mytilus cal-ifovnianus
shore crab—see Carcinus maenas
short-necked claFn--see Tapes japonioa
Sydney rock oyster—see Crassos-toea cormevcialis
tubificid worms—see Tubifex sp.
MAMMALS
Scientific Names
Alopex lagopus 40
Canis familiaris 40
Canis lupus 40
Erignatkus barbatus 40
Lutra aanadensis 42
Martes americana 72
Mustela vison 40, 42
Phoca hispida hispida 40
Rangifer tarandus 40
Rattus rattus 24
113
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MAMMALS (continued)
Common Names
arctic fox—see Alopex lagopus -
bearded seal—see Erignathus barbatus
caribou—see Rangifer tarandus
martin—see Martes americana
mink—see Mustela vison
otter—see Lutra eanadensis
rat—see Rattus rattus
ringed seal—see Phooa hispida hispida
sledge dog—see Can-Is famiHaris
wolf—see Can-Is lupus
AMPHIBIANS
Rana esaulenta 71
Rana tempoparia 71
ALGAE
Egregia laevigata 32
Navicula sp. 24
Scenedesmus sp. 56
114
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BACTERIA
Pseudomonas fluoresaens 37
Pseudomonas sp. 37
115
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