4>EPA
United States
Environmental Protection
Agency
Environmental Research
Laboratory
Gulf Breeze FL 32561
Research and Development
EPA/600/M-86/004 Feb. 1986
ENVIRONMENTAL
RESEARCH BRIEF
Critical Responses of
Populations of Crustacea to Toxicants
Charles L. McKenney, Jr.
Introduction
To adequately assess the biotic hazard of contaminants
entering the marine environment, suitable criteria must be
determined for detecting the ecological damage resulting
from long-term exposure to low concentrations of contami-
nants. Considering the close phylogenetic relationship
between Crustacea and the insect target for which pesti-
cides are directed, it is not surprising that crustaceans often
are more sensitive to pesticides than are other marine
organisms (Williams and Duke, 1979; Costlow, 1982).
Research at the Environmental Research Laboratory (ERL)
Gulf Breeze is directed toward determining appropriate
measurements for assessing the long-term effects of
pesticides on estuarine crustacean populations based on
both laboratory and field experimentation.
Toxicity tests in the last decade have established the mysid
shrimp, Mysidopsis bahia, as one of the most sensitive
membersof the estuarine community to pesticide exposure
(for a review see Nimmo and Hamaker, 1982) when simple
mortality is viewed as the major criterion. For the majority
of pesticides examined in life-cycle toxicity tests using this
estuarine crustacean, a sublethal reduction in reproductive
potential has proven to be the most sensitive criterion yet
determined for chronic biological effects in this zooplankton
species (Nimmo eta/., 1977, 1979, 1980, 1981).
Mysid reproduction, culminating in the release of fully
developed juveniles by brooding females, is, however, far
different from the reproductive process seen in benthic
crustacean populations in the estuarine community These
benthic populations, including both commercially and
ecologically important crabs and shrimp, reproduce by
releasing free-swimming pelagic larvae which undergo a
complex metamorphic process prior to settling into the
parental benthic population as young juveniles. Further-
more, larvae of estuarine crustaceans have been shown to
be particularly sensitive to environmental stress.
It is generally recognized that lower levels of biological
organization, the cellular and organismal levels, respond to
environmental stress long before higher levels such as
community and ecosystem levels (Figure 1) (National
Academy of Science, 1971; Waldichuk, 1979; Bayneef a/.,
1980; Kinne, 1980). Furthermore, ecologists have for many
years examined the productive processes of communities
and ecosystems by studying the underlying physiological
patterns of response of a species to environmental variables
throughout its life cycle (Mann, 1969; Winberg, 1971;
Steel, 1973, 1974; Grodzinski et a/., 1975).
The objective of the research summarized herein was to
provide information necessary to determine appropriate
responses for assessing the long-term effects of various
classes of pesticides on estuarine crustacean populations.
Dose-response relationships of pesticide toxicity and
individual physiological functions were examined and
compared for various life stages of estuarine mysids
(Mysidopsis bahia), grass shrimp (Palaemonetes pugio),
and mud crabs (Eurypanopeus depressus). Correlations
between physiological dysfunction of discrete life stages
and alterations in the ecological fitness of the population
should aid in the selection of sensitive, rapid, and inexpen-
sive monitoring tools for predicting chronic effects of
pesticides on pesticide-sensitive estuarine populations.
This research represents an ongoing effort by the ERL-Gulf
Breeze to identify particularly sensitive members of the
estuarine community to potential microcontamination by
specific classes of compounds and to provide the U.S.
Environmental Protection Agency (EPA) with ecologically-
sound test methods for assessing the ecotoxicological
hazard of these compounds to this vulnerable community.
-------
Figure 1. Rationale for the usefulness of monitoring sublethal physiological parameters as short-term predictive indicators of
long-term ecological damage by potential marine pollutants.
Natural Environmental Factors
Man-Made Microcontaminants
Detoxification
Disease Defense
Regulation
Adaptation
Energy
• Demanding
Processes
Hours
Days
Months
Years
Decades
Structural & Functional Changes
Biochemical
Cellular
Tissue
Organ
Organism
Reduction in Physiological Performance
(Reduced Stress Resistance, Growth, Reproduction)
Reduction in Ecological Potential
Consequences
Structural & Functional Changes
Population
Community
Ecosystem
Earlier efforts at this laboratory produced the first marine
invertebrate life-cycle toxicity test using the estuarine
mysid, Mysidopsis bahia (Nimmo et a/., 1977, 1979, 1 980,
1981; Nimmo and Hamaker, 1982). Recent emphasis has
shifted toward an appreciation of the functional role of
ecological indicator species and examination of the impact
of pollutant stress on community processes, resulting from
dysfunction among populations of these species both in
laboratory and field experimentation. Furthermore, an
increased awareness of environmental modification in the
toxic expression of potential microcontaminants has re-
sulted in laboratory examination of the mediation of toxicity
by physicochemical environmental factors.
Measurements of Chronic Toxicity to Endrin in
Mysidopsis bahia Populations
During a life-cycle toxicity test with Mysidopsis bahia
exposed to the organochlorinated insecticide, endrin,
various life stages were sub-sampled and measurements
made of metabolic and growth functions (Figure 2). These
individual physiological measurements were combined
into bioenergetic and physiological indices and compared
with alterations in survival and reproduction during the
chronic exposure period.
Concentrations of endrin that were acutely lethal (120
ng/L) stimulated respiration rates of newly released
juveniles after only one day of exposure (Figure 3). Exposure
to chronically lethal concentrations (60 ng/L) similarly
resulted in higher metabolic rates, but to a lesser extent.
Sublethal endrin exposure significantly reduced growth
rates of rapidly growing juveniles after four days exposure
to concentrations which were lethal after nearly three
weeks exposure (60 ng/L). In accordance with lower net
growth efficiencies (K2 values), increased metabolic de-
mands accompanying endrin exposure reduced the amount
of assimilated energy available for production of new
tissue.
Energy metabolism during juvenile stages of M. bahia was
based primarily on utilization of lipid substrates (as
indicated by the ratio of atoms of oxygen consumed to
atoms of nitrogen excreted). During the maturation period,
higher ammonia excretion rates and lower O:N ratios
suggested increased amounts of protein used as an energy
source. Reduced young production following chronic
exposure to endrin concentrations of 30 ng/L or greater
was correlated with increased lipid catabolism during
maturation of young mysids into adults (Figure 3). It was
postulated that enhanced energy demands, associated with
higher metabolic rates during sublethal endrin exposure,
favored usage of energy-rich lipid material at the cost of
shunting lipids away from gametogenesis and preparation
for reproduction.
-------
Figure 2. Life cycle of the estuarine mysid shrimp, Mysidopsis bah/a, depicting the various life stages subsampled for
physiological measurements during chronic pesticide exposure.
Multiple Broods
for
2-3 Months
First Brood Release
Day 20
Day 16
Young Adult
I .
Maturation
2° Sex Characteristics
Day 12
Day 10
Advanced Juvenile
Day 1
Early Juvenile
Day 4
Juvenile
Measurements of Chronic Toxicity to
Thiobencarb in Mysidopsis bahia Populations
A number of vital life processes of the estuarine mysid,
Mysidopsis bahia, were examined throughout its life cycle
during exposure to the carbamate herbicide, thiobencarb
(Figure4). Initial exposure of juvenile mysids to thiobencarb
resulted in elevated respiration rates. Concentrations of
thiobencarb which produced significant reductions in
population survival through a complete life cycle in
approximately 24 days (181 ng thiobencarb/L) significantly
stimulated respiration rates of juveniles after only four days
of exposure. Increased metabolic demands with sublethal
thiobencarb exposure (> 22 ng/L) reduced the amount of
assimilated energy available for production of newtissue by
juvenile mysids, resulting in retarded juvenile growth rates
after only four days of exposure. Modifications in the energy
metabolism of individual mysids exposed to thiobencarb
were related to decreases in total young production of
discrete populations. Greater usage of proteinaceous
substrates for energy metabolism during the maturation of
M. bahia juveniles was altered by exposure to high sublethal
concentrations of thiobencarb. Higher 0:N ratios during the
maturation of these thiobencarb-exposed mysids suggest a
greater reliance on the more energy-rich lipid substrates in
order to support the elevated rates of oxidative metabolism,
resulting in less lipid material being available for gamete
production.
From the responses of M. bahia to chronic thiobencarb
exposure through an entire life cycle, it may be concluded
that metabolic dysfunction in individual mysids preceded
population responses important in determining community
trophic patterns. Lower secondary production in a crus-
tacean population, as indicated in this study by retarded
mysid growth rates and inhibited reproductive rates, would
alter the energy-flow patterns between connected trophic
levels in the ecosystem. Although thiobencarb is directly
toxic to fish in low ng/L concentrations (Johnson and
Fenley, 1980; Schimmel et a/., 1983), the reduced second-
ary production of mysid populations with exposure to low
ng/L concentrations of thiobencarb could indirectly affect
fish populations dependent upon mysids as a food source
(Darnell, 1958; Odum, 1971; Chao and Musick, 1977;
Mauchline, 1980) and disrupt the balance of estuarine
food webs. Short-term measurements of altered metabolic
patterns in contaminated zooplankton, therefore, may offer
the potential of monitoring for and predicting ecological
disruptions in the estuarine ecosystem at higher levels of
biological organization, i.e., at the population or community
level.
-------
Figure 3. Summary of the effects of endrin on Mysidopsis bah/a exposed through an entire life cycle. VO2 = weight-specific
oxygen consumption rate; K2 = net growth efficiency (percentage of assimilated energy used for growth); O:N = atoms
of oxygen consumed to atoms of nitrogen excreted; VNH3 = weight-specific ammonia excretion rate.
130
110
90
QJ S'
g> -JQ
I
o
—I
50
30
10
VOi
\
Acute Lethality
Growth
K2
1
+
Growth
Chronic
Lethality
Young
Production
• 1
• VNH3
Early
Juvenile
(Day 1)
Juvenile
(Day 4)
Advanced Early
Juvenile Adult
(Day 10) (Day 16)
Life Stage (Day of Exposure)
Adult
(Day 20)
Figure 4. Summary of the effects of thiobencarb on Mysidopsis bahia exposed through an entire life cycle. Terms defined in
legend for Figure 3.
250
200
150
100
50
1
| Growth
V02
Growth
VOz
O:N
Chronic
Lethality
. r Young
~ T Production
Juvenile
(Day 4)
Advanced
Juvenile
(Day 10)
Early
Adult
(Day 16)
Adult
(Day 23)
Life Stage (Day of Exposure)
-------
Field-Study Confirmation of Toxicity
Measurements of Mysidopsis bahia to Fenthion
Low-level exposure to fenthion, following ground ULV
application of this organophosphate insecticide in various
mosquito control programs in Florida, produced both
increased mortality and sublethal growth retardation of
Mysidopsis bahia juveniles. Production of juvenile popula-
tions without continuous recruitment is the outcome of two
opposing processes: increased weight of individuals in the
population and decreased numbers of individuals in the
population due to mortality (Winberg, 1971). Increased
mortality and sublethal growth retardation of mysids
following low-level exposure to fenthion, therefore, would
result in reduced population production of this crustacean,
which serves as an important link in the estuarine food
chain between primary producers and commercially im-
portant fish utilizing the estuary as a nursery.
Significantly higher rates of oxygen consumption of
fenthion-exposed mysids eight days after the field spray
accompanied the reduced weights of the exposed mysids,
suggesting bioenergetic disruptions in mysids exposed
sublethally to fenthion in the field. Similar results have
been reported for M. bahia exposed to sublethal concentra-
tions of pesticides through an entire life cycle in the
laboratory (McKenney, 1982, 1985). Increased metabolic
demands on mysids exposed in the laboratory to pesticides,
as indicated by higher respiration rates, reduced the
amount of assimilated energy available for production of
new tissue, resulting in lower juvenile growth rates. These
field study results, therefore, confirm those of earlier
laboratory studies; short-term measurements of metabolic
dysfunction in mysids may predict altered production rates
in mysid populations.
Measurements of Chronic Toxicity to
Fenvalerate in Palaemonetes pugio Populations
Larvae of the estuarine grass shrimp, Palaemonetes pugio,
were reared in the laboratory from hatch through meta-
morphosis (Figure 5) under optimal salinity conditions
(20 o/oo) in a range of lethal and sublethal concentrations
of the pyrethroid insecticide, fenvalerate. Greater than 50
percent of the larvae exposed to measured concentrations
averaging 0.8 ng/L of fenvalerate died within four days of
continuous exposure. This concentration of fenvalerate
represents the lowest level of fenvalerate reported to
produce toxic effects on nontarget aquatic organisms.
Furthermore, since no mortality occurred for adult P. pugio
exposed to this same fenvalerate concentration, early larval
stages of estuarine crustaceans may be the most sensitive
to pesticide toxicity.
Continual exposure to the sublethal concentration of
fenvalerate (a nominal concentration of 1.6 ng/L) delayed
completion of metamorphosis for developing grass shrimp
larvae by nearly two days. Extension of this particularly
vulnerable pelagic phase in the life cycle may increase
predation pressure on the species. Increased predation on
larvae would reduce the number available for recruitment
into the parental benthic population or for dispersal and
establishment of new populations in less severe environ-
ments.
Figure 5. Life cycle of the ecologically important estuarine
grass shrimp, Palaemonetes pugio. This species
has been used successfully at ERL-Gulf Breeze
both in life-cycle and larval toxicity tests.
Life Cycle of Palaemonetes Pugio
Spawning
Juvenile Growth
Maturation
Larval
Development
Metamorphosis
to Postlarvae
Oxygen consumption rates of newly-released P. pugio
larvae were significantly higher after exposure for 24 hours
to fenvalerate concentrations which, after continual ex-
posure through the entire larval development, resulted in
significantly fewer larvae completing metamorphosis.
These results suggest that altered rates of respiration of
marine Crustacea may serve as rapid biological monitors of
detrimental effects of pesticide exposure to important
components of the estuarine community.
Upon completion of metamorphosis, postlarval P. pugio had
significantly higher rates of oxygen consumption in sub-
lethal concentrations of fenvalerate, which previously had
not altered larval metabolism. This species shifts from a
free-swimming pelagic larvae to benthic postlarvae when
metamorphosis is complete. The highly adsorptive nature
of fenvalerate (Schoor and McKenney, 1983) could have
resulted in adsorption onto the glass surface of the
exposure beakers during this study. Presumably benthic
postlarvae could have been more readily exposed to
fenvalerate adsorbed to the glass surface than larvae in the
water column, thus affording greater bioavailability and
increased metabolic sensitivity.
Responses of an estuarine organism to a toxicant are
dictated by the simultaneous influences of a number of
endogenous and exogenous variables (Figure 6). Tolerance
of osmotic stress is the most essential adaptation required
for a population to succeed in the fluctuating salinity
conditions of an estuary (for reviews see Lockwood, 1976;
Gilles and Jeuniaux, 1979). Moreover, metabolic compen-
sation to salinity by developing larvae of P. pugio may be
modified by sublethal toxicant exposure (McKenney and
Neff, 1981). Therefore, as an indication of the ecological
fitness of larval P. pugio, a secondary objective of this study
was to measure larval metabolism during osmotic stress to
-------
Figure 6. Responses of an estuarine organism to a toxicant
are dictated by the simultaneous influences of a
number of endogenous and exogenous variables,
including fluctuating salinity conditions.
Exogenous Factors
(i.e., temperature, food levels, dissolved oxygen, etc.)
Sublethal
Toxicant
Stress
Figure 7. Complete larval development of the estuarine
mud crab, Eurypanopeus depressus, through
metamorphosis.
Endogenous Factors
(size, sexual maturity, stage in life cycle, etc.)
determine if the ability of larvae to adapt to fluctuating
salinities was altered by sublethal exposure to fenvalerate.
Acute osmotic stress modified the metabolism of larval P.
pugio reared in sublethal, nominal fenvalerate concentra-
tions of 0.1 and 0.2 ng/L and these metabolic responses
varied with stage of development. After eight days of
exposure to fenvalerate, oxygen consumption rates were
elevated when larvae were acutely exposed to hypoosmotic
stress (1 Oo/oo S). Metabolic responses of premetamorphic
larvae to hyperosmotic stress (30 o/oo S) were also
modified by sublethal fenvalerate exposure. Alterations in
metabolic-salinity patterns of larval grass shrimp devel-
oping under sublethal fenvalerate concentrations suggest a
reduction in the ecological fitness of this sensitive life stage
manifested as a limitation in their capacity to adapt to the
fluctuating salinity conditions of estuarine waters.
Measurements of Chronic Toxicity to Lindane in
Eurypanopeus depressus Populations
The various life stages of an estuarine mud crab (Eury-
panopeus depressus), including the zoea, megalopa, and
adult stages (Figure 7), exhibited different response patterns
to lindane exposure, hypoosmotic stress, and interactions
between the pesticide and salinity stress. Larval stages of £.
depressus were more sensitive to lindane exposure than
adults. The larval 96-hour LC50 value for lindane exposure
was 0.66 IJQ/L as opposed to 25 /jg/L for adult crabs.
Long-term exposure to sublethal concentrations of the
organochlorinated insecticide, lindane, caused alterations
in ionic and osmotic regulatory ability and related com-
pensatory metabolic mechanisms in E. depressus. A
lindane exposure concentration of 1.45 uq/L reduced the
hemolymph osmotic concentrations m adult crabs. Chloride
ion regulation, however, was a more sensitive criterion,
being disrupted at a lindane exposure concentration of 0.70
/ug/L. A lindane exposure concentration of 0.01 ug/L
increased larval mortality and altered larval respiration and
ammonia excretion rates directly and in combination with
salinity stress. Increased larval sensitivity to pesticide
exposure may reduce larval survival/recruitment in pesti-
cide contaminated areas, resulting in altered distributional
patterns in adult benthic populations. Similarly, disruptions
of osmo-regulatory mechanisms may limit the natural
distribution of this species to areas with less salinity
variability.
Conclusions
Short-term measurements of altered metabolic patterns in
contaminated zooplankton offer the potential for monitoring
and predicting disruptions in estuarine ecosystems. Bio-
energetic events at the organismal level precede secondary
production rate changes at the population level. Laboratory
responses to both an organochlorinated pesticide (endrin)
and a carbamate pesticide (thiobencarb) were characterized
by modification of energy metabolism in individual mysids,
and these results preceded lower secondary production
rates caused by the same compounds. Sublethal exposure
of estuarine mysids to concentrations of these pesticides,
which initially elevated mysid respiration, eventually
inhibited growth and reproductive capacity of isolated
mysid populations in the laboratory. Results of these
laboratory studies were confirmed in a field study, indicating
that physiological measurements of metabolic dysfunction
in mysids exposed sublethally to pesticides may be used to
predict altered production rates in mysid populations.
Larvae of estuarine crabs and shrimp were more sensitive
to pesticide exposure than adults. Larvae of the estuarine
grass shrimp, Palaemonetes pugio, died upon exposure to
the lowest concentrations of a synthetic pyrethroid insecti-
cide (fenvalerate) found to produce toxic effects on non-
target aquatic organisms. Extremely low, sublethal levels of
fenvalerate (below the limit of analytical detection) reduced
the ecological fitness of larval estuarine grass shrimp
(Palaemonetes pugio) by limiting their capacity to adapt to
naturally occurring salinity fluctuations in estuarine waters.
Concentrations of the organochlorinated insecticide, lin-
dane, which were toxic to larval mud crabs (Eurypanopeus
depressus), were several orders of magnitude below those
-------
toxic to adult crabs. Moreover, chronic exposure to sublethal
concentrations of this pesticide altered ionic and osmoregu-
latory abilities and related compensatory metabolic mech-
anisms in larvae and adults of this estuarine crab, with
larvae being more sensitive than adults.
The research is described in the following publications:
McKenney, C. L., Jr. 1982. Interrelationships between
energy metabolism, growth dynamics, and reproduction
during the life cycle of Mysidopsisbah/a as influenced by
sublethal endrin exposure. In: Physiological Mechanisms
of Marine Pollutant Toxicity. W. B. Vernberg, A. Cala-
brese, F. P. Thurberg, and F. J. Vernberg (eds.). Academic
Press, New York, p. 447-476.
McKenney, C. L, Jr. and D. B. Hamaker. 1984. Effects of
fenvalerateon larval development of Palaemonetespugio
(Holthuis) and on larval metabolism during osmotic
stress. Aquatic Toxicology, 5:343-355.
McKenney, C. L., Jr. 1985. Associations between physio-
logical alterations and population changes in an estuarine
mysid during chronic exposure to a pesticide. In: Marine
Pollution and Physiology. F. J. Vernberg, F. P. Thurberg,
A. Calabrese, and W. B. Vernberg (eds.). University of
South Carolina Press, Columbia, SC, p. 397-418.
McKenney, C. L., Jr., E. Matthews, D. A. Lawrence, and M.
A. Shirley. 1985. Effects of ground ULV application of
fenthion on estuarine biota. IV. Lethal and sublethal
responses of an estuarine mysid. Journal ofFlorida Anti-
Mosquito Association, in press.
Shirley, M. A. and C. L. McKenney, Jr. 1986. Influence of
lindane on survival, osmoregulatory and metabolic
responses of the larvae and adults of the estuarine crab,
Eurypanopeus depressus. In: Physiological Effects of
Pollutants in Estuarine and Coastal Organisms. W. B.
Vernberg, A. Calabrese, F. P. Thurberg, and F. J. Vernberg
(eds.). University of South Carolina Press, Columbia, SC.
in press.
References
Bayne, B. L., J. Anderson, D. Engel, E. Gilfillan, D. Hoss, R.
Lloyd, and F. P. Thurberg. 1980. Physiological techniques
for measuring the biological effects of pollution in the
sea. Rapports et Proces-Verbaux des Reunions Conseil
International pour I'Exploration de la Mer, 179:88-99.
Chao, L. N. and J. A. Musick. 1977. Life history, feeding
habits, and functional morphology of juvenile sciaenid
fishes in the York River Estuary, Virginia. Fish. Bull.,
75:657-702.
Costlow, J. D., Jr. 1982. Impact of toxic organics on the
coastal environment. In: Impact of Man on the Coastal
Environment. T. W. Duke (ed.). EPA/600/8-82/021,
Washington, DC, p. 86-95.
Darnell, R. M. 1958. Food habits of fishes and larger
invertebrates of Lake Pontchartrain, Louisiana. Contrib.
Mar. Sci., 5:353-416.
Gilles, R. and Ch. Jeuniaux, 1979. Osmoregulation and
ecology in media of fluctuating salinity. In: Mechanisms
of Osmoregulation in Animals. R. Gilles (ed.). John Wiley
and Sons, Chichester, p. 581-608.
Grodzinski, W., R. Z. Klekowski, and A. Duncan. 1975.
Methods for Ecological Bioenergetics. Blackwell Scien-
tific Publications, Oxford, 367 pp.
Johnson, W.W. and M.T. Fenley. 1980. Handbook of Acute
Toxicity of Chemicals to Fish and Aquatic Invertebrates.
Resource Publication 137. U.S. Fish and Wildlife Service.
Washington, DC, 98 pp.
Kinne, O. 1980. Summary of symposium papers and
conclusions. In: 14th European Marine Biology Sym-
posium: Protection of Life in the Sea. O. Kinne and H.-P.
Bulnhiem (eds.). Helgol. wiss. Meeres. 33:732-761.
Lockwood, A. P. M. 1976. Physiological adaptations to life
in estuaries. In: Adaptation to Environment. R. C. Newell
(ed.). Butterworths, London, pp. 315-392.
Mann, K. H. 1969. The dynamics of aquatic ecosystems. In:
Advances in Ecological Research. J. B. Cragg (ed.).
Academic Press, London, pp. 1-81.
Mauchline, J. 1980. The biology of mysids and euphausiids.
Part 1. The biology of mysids. Adv. Mar. Biol., 18:1-369.
McKenney, C. L., Jr. 1982. Interrelationships between
energy metabolism, growth dynamics, and reproduction
during the life cycle of Mysidopsis bahia as influenced by
sublethal endrin exposures. \n:PhysiologicalMechanisms
of Marine Pollutant Toxicity. W. B. Vernberg, A. Cala-
brese, F. P. Thurberg, and F. J. Vernberg (eds.). Academic
Press, New York, pp.447-476.
McKenney, C. L., Jr. 1985. Associations between physio-
logical alterations and population changes in an estuarine
mysid during chronic exposure to a pesticide. In: Marine
Pollution and Physiology. F. J. Vernberg, F. P. Thurberg,
A. Calabrese, and W. B. Vernberg (eds.). University of
South Carolina Press, Columbia, SC, pp 397-418.
McKenney, C. L., Jr. and J. M. Neff. 1981. The ontogeny of
resistance adaptation and metabolic compensation to
salinity and temperature by the caridean shrimp,
Palaemonetespugio, and modifications by sublethal zinc
exposure. In: Biological Monitoring of Marine Pollutants.
F. J. Vernberg, A. Calabrese, F. P. Thurberg, and W. B.
Vernberg (eds.). Academic Press, New York, pp. 205-240.
National Academy of Science. 1971. Marine Environmental
Quality. National Academy of Science, Washington, DC,
107pp.
Nimmo, D. R. and T. L. Hamaker. 1982. Mysids in toxicity
testing—a review. Hydrobiologia, 93:171-178.
Nimmo, D. R., T. L. Hamaker, J. C. Moore, and C. A.
Sommers. 1979. Effect of diflubenzuron on an estuarine
crustacean. Bull. Environ. Contam. Toxicol., 22:767-770.
Nimmo, D. R., T. L. Hamaker, J. C. Moore, and R. A. Wood.
1980. Acute and chronic effects of Dimilin on survival
and reproduction of Mysidopsis bahia. In: Aquatic
Toxicology, ASTM STP 707. J. G. Eaton, P. R. Parrish, and
A. C. Hendricks (eds.). American Society for Testing and
Materials, Philadelphia, pp. 366-376.
Nimmo, D. R.,T. L. Hamaker, E. Matthews, and J. C. Moore.
1981. Overview of the acute and chronic effects of first
and second generation pesticides on an estuarine mysid.
In: Biological Monitoring of Marine Pollutants. F. J.
Vernberg, A. Calabrese, F. P. Thurberg, and W. B.
Vernberg (eds.). Academic Press, New York, pp. 3-19.
Nimmo, D. R., L. H. Bahner, R. A. Rigby, J. M. Sheppard, and
A. J. Wilson. 1977. Mysidopsis bahia: An estuarine
species suitable for life-cycle toxicity tests to determine
the effects of a pollutant. In: Aquatic Toxicology and
Hazard Evaluation, ASTM STP 632. F. L. Mayer and J. L.
Hamelink (eds.). American Society for Testing and
Materials, Philadelphia, pp. 109-116.
•&U. S. GOVERNMENT PRINTING OFFICE:1986/646-l 16/20776
-------
Odum, W. E. 1971. Pathways of Energy Flow in a South
Florida Estuary. University of Miami Sea Grant Program,
Sea Grant Technical Bulletin #7, Miami, 162 pp.
Schimmel, S. C., R. L. Garnas, J. M. Patrick, Jr., and J. C.
Moore. 1983. Acute toxicity, bioconcentration, and
persistence of AC 222, 705, benthiocarb, chloropyrifos,
fenvalerate, methyl parathion, and permethrin in the
estuarine environment. J. Agric. Food Chem., 31'104-
113.
Schoor, W. P. and C. L. McKenney, Jr. 1983. Determination
of fenvalerate in flowing-seawater exposure studies.
Bull. Environ. Contam. Toxicol., 30:84-92.
Steel, J. H. 1973. Marine Food Chains. Oliver and Boyd,
Edinburgh, 552 pp.
Steel, J. H. 1974. The Structure of Marine Ecosystems.
Harvard University Press, Cambridge, MA, 128 pp.
Waldichuk, M. 1979. Review of the problem. In: The
Assessment of Sublethal Effects of Pollutants in the Sea.
H. A. Cole (ed.). The Royal Society, London, pp. 1 -26.
Williams, A. B. and T. W. Duke. 1979. Crabs (Arthropoda:
Crustacea: Decapoda: Brachyura). In: Pollution Ecology of
Estuarine Invertebrates. C. W. Hart, Jr. and S. L. H. Fuller
(eds.). Academic Press, New York, pp. 171 -233.
Winberg, G. G. 1971. Methods for the Estimation of
Production of Aquatic Animals. Academic Press, New
York, 175 pp.
United States
Environmental Protection
Agency
Center for Environmental Research
Information
Cincinnati OH 45268
Official Business
Penalty for Private Use $300
EPA/600/M-86/004
000032" PS
U S ENVIR PROTECTION AGENCY
REGION 5 J-IBRARY
?10 S DEARSORN STREtT
CHICAGO IL 60604
------- |