water quality requirements for reuse systems
TRANSCRIPT
Water quality requirements for reuse systems
John Colt *
Northwest Fisheries Science Center, National Marine Fisheries Service, 2725 Montlake Blvd. East, Seattle, WA 98112-2097, USA
Abstract
Water quality criteria for aquaculture systems have typically considered parameters such as temperature, dissolved oxygen,
total gas pressure, ammonia, and nitrite. Many of the published criteria are derived for environmental protection of a wide range
of species and life stages. These criteria may not be appropriate for a single species and life stage, especially in commercial
applications. The value of a given water quality criterion may depend strongly on the species, size, and culture objectives. In
water reuse systems, fine solids, refractory organics, surface-active compounds, metals, and nitrate may become important. The
limiting factors in very high intensity reuse systems are not entirely understood at this time. Development of more relevant water
quality criteria for reuse systems will require production-scale trials. Separate water quality criteria for biofilter operation are
also needed.
Published by Elsevier B.V.
Keywords: Water quality criteria; Reuse; Fine solids; Surface active compounds; Carbon dioxide
www.elsevier.com/locate/aqua-online
Aquacultural Engineering 34 (2006) 143–156
1. Introduction
Two general types of water quality criteria are
needed for reuse systems: criteria for the culture
species and criteria for the operation of unit processes
and unit operations. This second type of water quality
criteria is not needed for flow-through or pond
production systems.
While there is much information in the literature on
water quality criteria, much of this information may
not be appropriate for a specific aquaculture venture.
Published criteria may be formulated to protect human
public health, prevent undesirable or nuisance aquatic
life, or protect free-living aquatic animals. Water
* Tel.: +1 206 860 3243; fax: +1 206 860 3467.
E-mail address: [email protected].
0144-8609/$ – see front matter. Published by Elsevier B.V.
doi:10.1016/j.aquaeng.2005.08.011
quality criteria for environmental protection must
consider the effects on a wide range of species and life
stages. A given culture system is designed for a small
number of species and typically the more sensitive life
stages (reproduction and early larval form) are raised
in separate systems. The biomass of broodstock and
larvae is small and the cost of maintaining high water
quality in these systems is relatively small. The cost of
maintaining water quality in growout systems has a
much more significant impact on overall production
economics. In addition, the culture objectives (food
production versus endangered species enhancement)
may also change the specific value selected for a
criteria.
Most toxicity studies are conducted on juvenile
animals for a relatively short time and expose the test
organisms to constant concentrations while maintain-
J. Colt / Aquacultural Engineering 34 (2006) 143–156144
ing other parameters within an acceptable range. The
extrapolation of these types of experiments to the
entire production cycle and to combinations of
environmental parameters (for example, high total
ammonia and carbon dioxide in combination with
supersaturated dissolved oxygen) is difficult if not
impossible.
The purpose of this paper is to document how
published water quality criteria are determined, to
explain why published criteria may not be appropriate
for reuse systems, and to suggest how more
appropriate objective-specific criteria may be devel-
oped.
2. Characteristics of toxicity testing
Water pollution concerns have resulted in the
development of standardized toxicity testing protocols
for aquatic animals (for example, see Clesceri et al.,
1998; Committee on Methods, 1975; Peltier, 1978).
Most toxicity studies are single-factor experiments
with constant exposure concentrations. An example of
this type of experiment would be exposure of groups
of juvenile fish to a series of constant ammonia
concentrations while maintaining acceptable levels of
dissolved oxygen, carbon dioxide, total gas pressure,
pH, and temperature. Multifactor aquatic exposure
experiments or variable exposure concentrations are
difficult to conduct because of complexity of
experimental controls and the statistical need for
replication.
Some acute toxicity experiments are relatively
short-term (24–96 h) but sublethal exposure trials
commonly require 30–90+ days for aquatic organisms.
One classic study on the sublethal effects of ammonia
on rainbow trout (Oncorhynchus mykiss) throughout
their life cycle required 5 years to complete (Thurston
et al., 1984). At the time this research was published,
the authors thought that this was the only full life-
cycle toxicity test of ammonia to any fish species and
the only report of a life-cycle toxicity test on rainbow
trout for any toxicant. In addition to the life-cycle test,
USEPA also defines partial life cycle and early life-
stage experiments (USEPA, 1985). Because of the
difficulty of working with long-generation time
species (and most commercially important species),
there is an increasing tendency to work with smaller
aquatic organisms such as zebra fish (Brachydanio
rerio), rotifers, and daphnia.
For acute mortality tests, it is common to report the
50% mortality values for a given time (24 h LC50,
48 h LC50, 96 h LC50). For sublethal tests, the
response at each concentration may be tested for
significance using common statistical tests and three
specific parameters are commonly reported in toxicity
literature (Mayes et al., 1986):
� T
he no-observable-effects concentration (NOEC):The high concentration tested at which some
selected effect failed to be produced within some
specified period of exposure.
� T
he lowest-observable-effect concentration(LOEC): The lowest concentration at which a
selected effect is observed.
� T
he maximum-acceptable-toxic concentration(MATC): The geometric mean of NOEC and LOEC.
A given parameter can have an impact below the
NOEC concentration. The lack of statistical signifi-
cance at lower concentrations may be a result of
inadequate replication to detect the small differences
between the means of low treatments and the controls.
The shape of the toxicity response curve in this range
is subject to great debate in the animal and human
toxicity fields.
3. Water quality criteria in the United States
Section 304(a)(1) of the Clean Water Act (33 USC
1314(a)(1)) requires the United States Environmental
Protection Agency (USEPA) to publish and periodi-
cally update ambient water quality criteria. ‘‘Water
quality criteria developed under Section 304(a) are
based solely on data and scientific judgments on the
relationship between pollutant concentrations and
environmental and human health effects. Section
304(a) criteria do not reflect consideration of
economic impacts or the technological feasibility of
meeting the chemical concentrations in ambient
water.’’ (USEPA, 2002). With respect to trace
contaminate concentrations such as methyl mercury,
DDT, dioxin, etc., the USEPA regulates the consump-
tion of sport caught fish and invertebrates while the
U.S. Food and Drug Agency (FDA) regulates
J. Colt / Aquacultural Engineering 34 (2006) 143–156 145
commercially marketed fish and seafood products.
The action levels and recommended consumption
levels are significantly different between the two
agencies, a source of great confusion to the general
public.
The USEPA has published a series of ambient water
criteria books that are commonly referred to by their
color (‘‘Green Book’’, ‘‘Blue Book’’, ‘‘Red Book’’,
and ‘‘Gold Book’’). The last published as a book was
the ‘‘Red Book’’ (USEPA, 1976). The criteria were
simple numerical criteria (‘‘0.02 mg/L (as un-ionized
ammonia) for freshwater life’’) and in many cases
were computed from lethal tests and an application
factor of 10–100. The ‘‘Gold Book’’ (USEPA, 1986)
was published in a three ring binder and annually
updated for some period of time. The procedure used
to develop new water quality criteria was formalized
in USEPA (1985). Two different criteria are devel-
oped:
Criterion maximum concentration (CMC): 1 h
exposure.
Criterion continuous concentration (CCC): 4 day
exposure.
Separate CMC and CCC criteria may be developed
for freshwater and saltwater applications. The actual
criterion is stated as:
The procedures described in the ‘‘Guidelines for
Deriving Numerical National Water Quality
Criteria for the Protection of Aquatic Organisms
and Their Uses’’ indicate that, except possibly
where a locally important species is very
sensitive, (insert ‘‘freshwater’’ or ‘‘saltwater’’)
aquatic organisms and their uses should not be
affected unacceptably if the 4-day average
concentration of (insert name of material) does
not exceed (insert CCC value) mg/L more than
once every 3 years on the average and if the 1 h
average concentration does not exceed (insert
CMC value) mg/L more than once every 3 years
on the average.
The scientific basis for the selection of a 3 year
reoccurrence interval is not entirely convincing. Not
all of water quality criteria listed in the ‘‘Gold Book’’
or the latest published summary (USEPA, 2002) have
been developed using the published protocols
(USEPA, 1985). The criteria development document
(USEPA, 1985) is currently being updated and
revised.
The CMC and CCC for some parameters may be
written as a function of hardness or pH. Because the
criteria must be legally defensible, the procedure for
the computations (USEPA, 1985) is quite detailed in
the potential impacts studied as well as the number of
different species required, but in general, the selected
criterion will protect 95% of the species considered.
The most current water quality criteria publication
is USEPA (2002) and is more of a summary and source
of information on each parameter. Details on the basis
of each criterion may found in the footnotes, cited
references, or in some cases, sections in the previously
published ‘‘Gold Book’’. It may be necessary to refer
to more than one document for complete information.
4. Selection of water quality criteria for waterreuse applications
The selection of water quality criteria for water
reuse may be based on published environmental
protection criteria, species-specific publications, or
aquaculture books, or may require development of site
and species-specific criteria. The selection of criteria
depends strongly on the species reared, culture
objectives, and regulatory requirements. Basic infor-
mation on typical water quality parameters will not be
presented in this article, as this information is readily
available in other publications. The next section,
presents detailed information on parameters of critical
importance in reuse systems.
4.1. Environmental protection criteria
Water quality criteria published for environmental
protection (Alabaster and Lloyd, 1980; McKee and
Wolf, 1968; USEPA, 1986, 2002) are an invaluable
source of information on potential impacts of water
quality parameters. In many cases, these published
criteria should not be used directly in the design and
operation of reuse systems.
A criterion designed to protect a broad range of
species and life stages is likely to be too conservative
for someone rearing 10–20 cm tilapia or rainbow
trout. The impact of a parameter on broodstock, eggs,
J. Colt / Aquacultural Engineering 34 (2006) 143–156146
or larvae is not important if they are not reared at a
given site.
Published criteria may be based on public health
considerations and critical water quality parameters
for aquatic culture conditions may be lacking. The
criterion for nitrate (10 mg/L total nitrate nitrogen) in
USEPA (2002) is based on potential impacts on human
infants. No freshwater or seawater water quality
criteria are developed for either nitrate or nitrite
(USEPA, 2002), two very important parameters in
reuse systems.
Most of the published studies used to development
water quality standards are single-factor experiments
with constant exposure concentrations. These types of
exposures seldom occur in real systems. A real world
evaluation of ammonia toxicity might test the impact
of diel varying ammonia concentration on the growth
of 300–400 g channel catfish under high carbon
dioxide levels (40 mg/L free carbon dioxide) when
DO is maintained at 120% of saturation with pure
oxygen, and total gas pressure is 110%.
Much effort has been expended in trying to predict
joint toxicity of several parameters. For some
parameters, it is possible to estimate joint toxicity
under some limited range of conditions but in general,
the results of single-factor experiments cannot be used
to predict the joint impacts of several water quality
parameters. These types of experiments are much
more relevant to commercial conditions but are also
much more difficult to conduct and publish.
Much of the published information is from
relatively short-term experiments and does not cover
the full production cycle. While there is documenta-
tion on the impacts of fixed and variable ammonia
concentrations on fingerling channel catfish (1–10 g)
(Colt and Tchobanoglous, 1978; Hargreaves and
Kucuk, 2001), there is little documentation for larger
fish (>20–400 g). On the other extreme, it is hard to
apply the multi-generation rainbow trout exposure
information (Thurston et al., 1984) to production
growout systems because the broodstock, eggs, and
larvae were exposed to the same concentrations as the
fingerlings and larger fish. Because of the importance
of eggs and larvae and their relative small total
biomass, it is relatively inexpensive to provide these
live stages with exceptional water quality. Costs only
become important with larger sized animals and
higher biomasses.
Most published water quality criteria are based on
a ‘‘no effect’’ level. If the parameter is less than the
criteria, it is assumed that the parameter should have
no effect on the specific animal/life state. For many
parameters such as ammonia, nitrite, or dissolved
oxygen, it is necessary to know not only the ‘‘no
effects’’ levels but also the functional relationship
between these parameters and parameters such as
growth rate or product quality. The design level
will depend both on the effects of these parameters
on the culture animals and the costs of maintaining a
given level. For other parameters such as heavy
metals, chlorine residual, or biocides criteria
based on a no-effects concentration may be appro-
priate.
4.2. Fisheries and aquaculture and books
Species handbooks, fish hatchery manuals, or
aquaculture books are an excellent source of
information for water quality information and current
culture protocols. Some of the most helpful references
for species commonly reared in the Americas are
presented below:
Genus, species, or group
ReferenceSalmonids
Barton (1996), Piper et al. (1982),Sigma (1983), Wedemeyer (1996)
Temperate basses
Tomasso (1997)Channel catfish
Boyd and Tucker (1998), Stickney(1993)
Black basses
Williamson et al. (1993)Sunfishes
Williamson et al. (1993)Walleye
Nickum and Stickney (1993)Pikes
Westers and Stickney (1993)Tilapia
Costa-Pierce and Rakocy (1997)Sturgeon
Conte (1988)Marine fish
Poxton and Allouse (1982)Marine larval fishes
Brownell (1980a,b)General
Wickins (1981)While these sources are very useful, it is impor-
tant to realize that in general, they will depend
on primary data with the same limitation as
discussed previously. Commonly, much of informa-
tion contained in these sources is based on the
experiences and practices of state, tribal, and federal
hatchery programs. Current information from large-
scale commercial enterprises is very difficult to
find.
J. Colt / Aquacultural Engineering 34 (2006) 143–156 147
Table 1
Important factors in the selection of water quality criteria for aquatic culture systems
Type of criteria Example
Lethal effects Important in the design of backup systems, transport systems, and
holding system at processing plants
Sublethal effects
Growth Basic parameter in production systems
Fin quality and appearance Importance for products sold alive and for some products consumed
in a specific manner
Tissue quality Product quality (texture, taste, and odor) for human consumption
Physiological quality Smoltification in anadromous salmonids
Behavioral and fish health quality Ability of stocked animals to adapt and survive after planting
(enhancement and restoration)
Endocrine, reproductive, or immune
impacts in animals and humans
Caused by endocrine disrupters (environmental estrogens or
estrogenic xenobiotics)
Regulatory requirements
Phosphorous, nitrogenous compounds,
BOD, suspended solids, and chemical releases
Effluent discharge requirements under the Clean Water Act
Trace contaminates in tissue Levels of methymercury, PCB, DDT, or dioxins may limit human
consumption (amount or frequency)
Disease causing microorganisms Hepatitis A, Vibrio spp., E. coli
4.3. Development of facility specific water quality
parameters
Several online databases such as BIOSIS (Biological
Abstracts), Aquaculture (NOAA), and ASFA (Aquatic
Sciences and Fisheries Abstracts) are convenient
sources of information and citations. These databases
can be searched by author, species, and for a specific
parameter. Many of the supporting documents used by
the USEPA to develop water quality criteria are
available over the web (www.epa.gov/waterscience/
standards/).
The selection of criteria for the design of culture
systems may depend strongly on the objectives of the
project, the species, and life stage reared. Factors that
may be important in the selection of criteria are
presented in Table 1. In production systems, the effects
of a given parameter on growth is probably the most
important consideration and a simple linear (or
polynominal) growth curve can be fitted to many
growth studies:
Growth rate ð% of maximumÞ ¼ 100� m� YGrowth rate ð% of maximumÞ ¼ 100� a� Y � b� Y2
Growth rate ð% of maximumÞ ¼ 100� a� Y � b� Y2
where m is the slope of the growth curve; a, b, c are the
regression coefficients; Y is the value of the specific
parameter.
Assuming that growth information is available, is it
relatively simple to compute the selected regression
curves with commonly available statistical or graph-
ing programs, but selection of the appropriate value of
Y will still require judgment and perhaps validation.
The physiological and behavioral quality of fish
may be more important if fish are to be released
to nature. The design of backup water or aeration
systems, transport systems, or holding vats at pro-
cessing plants may be designed to prevent significant
mortality. Animals are not held in these types of
systems long enough for sublethal effects to become
important. Discharge of waters from intensive culture
systems may be regulated by State and Federal
agencies.
Because of economic pressures, commercial
producers tend to push the envelope of acceptable
water quality and culture practices. Changes in
ðlinearÞðsecond order polynominalÞ
� c� Y3 ðthird order polynominalÞ
J. Colt / Aquacultural Engineering 34 (2006) 143–156148
technology (better feeds, pure oxygen, ozone disin-
fection, etc.) allow increases in density or loading that
were unachievable in the past. Because of these
changes in basic rearing conditions and the previously
discussed differences in the objectives of the criteria
(see Table 1), the selection of appropriate water
quality criteria for a given production system/species/
life stage requires serious study, analysis, and field
verification. Meade (1985) concluded that ‘‘a truly
safe, maximum acceptable concentration of un-
ionized, or total, ammonia for fish culture systems
is not known.’’ . . . The apparent toxicity of ammonia is
extremely variable and depends on more than the
mean or maximum concentration of NH3.
Meade (1985) also suggested the following
approach to development of production water quality
parameters:
1. E
Tab
Che
Typ
Me
Dis
Tox
Dis
Nu
Oth
a
stimate maximum or safe concentrations based on
available information.
2. D
evelop production indexes based on holisticdata collected by monitoring a number of rearing
systems.
le 2
mical and physical parameters important to culture animals and/or di
e Parameter
tabolic wastes Ammonia
Nitrite
Nitrate
Pheromones
Fecal wastes (large solids)
Fine solids
solved gases Oxygen
Carbon dioxide
Hydrogen sulfide
Gas supersaturation
ics Heavy metals
Chlorine
Ozone
Biocides, toxic organics
solved or suspended material Salinity/total dissolved solids
Solids/turbidity
pH
trients P compounds
er parameters Surface-active compounds
Color compounds
A, fixed criterion; V, variable criterion; I, indicator criterion.
3. A
djust safe concentrations based on monitorinformation and validate with additional monitor-
ing.
Development of species or system specific water
quality criteria is time consuming, expensive, and may
be difficult to publish in a peer-reviewed journal.
A summary of important water quality parameters
is presented in Table 2. Each parameter is classified in
terms of: (1) cost implications, (2) type of criteria, and
research priority. Not all of the water quality
parameters have major cost implications in reuse
systems. Each parameter is further classed in terms of
a fixed criterion, a variable criterion, or an indicator
criterion.
A variable criterion is needed for parameters that
have significant cost implications. The maintenance of
ammonia, nitrite, fecal solids, carbon dioxide, and
surface-active compounds may have the greatest
costs implication in design and operation of reuse
systems. For these parameters, it necessary to consider
tradeoffs between the selected water quality criteria
and operating costs. For parameters with less cost
scharge in aquatic systems
Cost implications Type of criteriaa Priority in reuse
Yes V, I HYes V, I H
A H? H
Yes A
Yes V H
Yes V HYes V H
A
A
A HA
A
A
A
A
A
A
Yes I HI H
J. Colt / Aquacultural Engineering 34 (2006) 143–156 149
Table 3
Chemical and physical parameters important to biofilter operations
Parameter Implications
Nitrate A minimum level of nitrate will prevent formation of hydrogen sulfide in ponds subjected to
anaerobic conditions
Oxygen Nitrification stops at low dissolved oxygen
Therapeutic drugs and chemicals Drugs and chemicals can have a serious impact on nitrification
pH (and alkalinity) The nitrification process slows down at high and low pHs
Salinity Different bacteria are responsible for nitrification in freshwater and seawater. Rapid changes in
salinity can reduce the rate of nitrification for a period of time
implications, it may be possible to select a single fixed
criteria. An indicator criteria is a parameter that is
correlated with the critical water quality parameters
but is easier to measure or observe. For example, it
may be desirable to keep influent ammonia and nitrite
concentration in the undetectable range (<0.01 mg/L)
as a general measure of water quality in broodstock or
larval systems. An increase of ammonia to 0.15 mg/L
indicates a problem with the biofilter performance that
may adversely influence a number of other water
quality parameters that are more difficult (or
impossible) to accurately monitor. Changes in water
color or surface tension may be important indicator
variables in reuse systems.
4.4. Water quality parameters for biofilter
operations
Up to this point, the water quality criteria
parameters have been based on the needs of the
culture animal. It is also necessary to consider the
impacts of water quality on biofilter operation
(Table 3). Detailed information will be presented on
these parameters in other articles in this special issue.
5. Critical water quality parameters in reuse
systems
Compared to flow-through or ponds, reuse systems
typically have significantly reduced make-up flows
that can result in the build-up of some compounds.
Also, the ability to independently control parameters
such as DO or chloride ion concentration, may allow
culture animals to tolerate higher levels of other water
quality parameters (compared with other culture
types). This section will discuss water quality criteria
for parameters critical to the successful operation of
reuse systems. Emphasis will be placed on areas of
uncertainty, rather that review the large body of
general published literature on these parameters.
5.1. Ammonia
Detailed information on the toxicity of ammonia to
fish has been reviewed by Tomasso (1994). The
toxicity of ammonia is generally assumed to be due to
the concentration of the un-ionized ammonia mole-
cule (NH3) because of its ability to move across
cell membranes. The concentration of NH3 can be
computed from the following equation:
½NH3 � N� ¼ ½TAN�1þ 10ðpKa�pHÞ
where [TAN] is the measured concentration of total
ammonia nitrogen (mg/L); pKa, the acidity constant
for the reaction (9.40 at 20 8C); pH, the measured pH
of the solution; [NH3 � N], computed concentration
of NH3 (mg/L or mg/L).
While TAN, pH, and temperature determine the
concentration of un-ionized ammonia, pH appears to
have a impact on ammonia independent of the above
equation, which suggests that the ionized ammonium
ion (NH4+) has some toxicity. For a TAN = 5.0 mg/L,
the concentration of un-ionized ammonia in mg/L is
presented below as function of pH:
pH
NH3 � N (mg/L)9.00
14308.00
1917.00
206.00
25.00
0.24.00
0.02J. Colt / Aquacultural Engineering 34 (2006) 143–156150
At a pH of 9.0 and TAN = 5 mg/L, typical fish
would be dead in hours, while with pH less than 6.0,
ammonia would have negligible impacts. The ability
to modify culture pH has the ability to maintain low
un-ionized ammonia concentrations in the system
while achieving high TAN removal rates because of
the high TAN concentrations. There is also some
evidence that pH adjustment (or pH fluctuations) can
be used to control some pathogens in reuse systems
(Dallas Weaver, personal communication).
The above equation (and many published tables)
over-estimates the un-ionized ammonia concentration
by 10–20% in waters with high total dissolved solids
concentrations (Messer et al., 1984). Non-ideal
correction to this equation can be readily made if
the ionic composition of the water is known. The
computation of un-ionized ammonia in seawater is
complicated by the fact the pKa values for seawater
(Whitfield, 1978; Khoo et al., 1977) are based on a
different pH scale (Hansson, 1973). The data
presented by Millero (1986) can be used to convert
between the two pH scales. The computer program
developed by Hampson (1977) clearly stated that the
Hansson pH must be used, but Bower and Bidwell
(1978) did not distinguish between the two pH scales.
The use of conventional pH values in the equations
developed by Whitfield (1978) or Khoo et al. (1977)
can over-estimate the un-ionized ammonia concentra-
tion by up to 43% (20 8C, 35 g/kg).
Ammonia appears to have a direct effect on the
growth of aquatic animals. Increasing the un-ionized
ammonia concentration produces a linear reduction in
growth of channel catfish (Ictalurus punctatus) (Colt
and Tchobanoglous, 1978). Ammonia can have a
serious effect on the incidence of disease, especially
under less optimum conditions of temperature
and dissolved oxygen. Low DO and variable NH3
concentrations can increase the toxicity of ammonia
while increasing salinity and sodium levels will reduce
its toxicity.
The commonly used un-ionized ammonia criterion
in salmonid culture of 12.5 mg/L (Westers, 1981) is
based on gill damage attributed to ammonia exposure
(Smith and Piper, 1975). Recent work discounts the
impact of ammonia on gill damage and suggests the
un-ionized ammonia criteria could be at least 40 mg/L
or higher (Meade, 1985) for state and federal
hatcheries. For commercial production, the water
quality criterion for un-ionized ammonia may be even
higher than 40 mg/L.
5.2. Nitrite
Nitrite is the ionized form of the relatively strong
acid, nitrous acid. The concentration of nitrous acid
can be computed from the following equation:
½HNO2 � N� ¼ ½TNN�1þ 10ðpH�pKaÞ
where [TNN] is the measured concentration of total
nitrite nitrogen (mg/L); pKa, acidity constant for the
reaction (3.38 at 20 8C); pH, measured pH of the
solution; [HNO2 � N], computed concentration of
HNO2 (mg/L or mg/L).
For a TNN = 1.0 mg/L, the concentration of nitrous
acid nitrogen in mg/L is presented below as function of
pH:
pH
HNO2 � N (mg/L)9.00
0.00248.00
0.0247.00
0.2406.00
2.405.00
284.00
166At normal pHs, very little nitrous acid is present.
Nitrous acid is freely diffusible across gill membranes
while nitrite is not (Tomasso, 1994) but nitrite can be
actively transported across gill membranes by the
mechanism that normally transports chloride inward.
The addition of chloride ions protect fish from the
toxicity of nitrite by competitively excluding nitrite
from uptake by the chloride active transport mechan-
ism in the gills. In pond culture of channel catfish, it is
common to add NaCl to maintain a chloride:nitrite
ratio of 4:1 on a molar basis or 10.1:1 on a weight basis
(Schwedler and Tucker, 1983).
High concentration of chloride in seawater may not
be protective for all invertebrates (Tomasso, 1994).
While the concentration of un-ionized nitrous acid
increases at lower pH, Lewis and Morris (1986)
concluded that there is no evidence of increased nitrite
toxicity at lower pHs. Because of the effects of buffer
addition and acclimation issues in the experiments
reviewed by Lewis and Morris (1986), the effects of
J. Colt / Aquacultural Engineering 34 (2006) 143–156 151
pH on nitrous acid toxicity may have been confounded
(Tomasso, 1994). If the pH of a reuse system is
lowered, the toxicity of total nitrite nitrogen may be a
more important problem even if chloride is added.
5.3. Nitrate
The toxicity of nitrate to freshwater fish is very low
(96 h LC50s >1000 mg/L as N) and may be related to
potential osmoregulation problems. In systems with
high nitrate concentrations, reduction of nitrate to
nitrite can occur in anaerobic areas and some nitrate
exposure studies may be confounded by undocumen-
ted nitrite levels.
The nitrate-N concentrations should be less than
500 mg/L for large marine fish (Pierce et al., 1993),
but marine tropical fish such as anemonefish
(Amphiprion ocellaris) are more sensitive and a
criterion of 20 mg/L was suggested for this species
(Frakes and Hoff, 1982). Walsh et al. (2002)
recommended a criterion of 50 mg/L as N for the
rearing of squid.
5.4. Pheromones, endocrine disrupters, and other
toxic chemicals
Chemical communication between individuals of
the same species is due to the secretion of chemical
compounds called pheromones. Pheromones play a
significant role in many aspects of behavior and
development such as homing of migratory fish, alarm
reactions, pair formation and spawning, and reduction
of growth due to ‘‘crowding factors’’ (Solomon,
1977). The impacts of these chemicals may be
important in the maturation of some fish species held
in reuse systems, although documentation is currently
lacking.
Endocrine-disrupting chemicals (EDCs) encom-
pass a wide variety of chemical, including natural and
synthetic hormones, plant constituents, pesticides,
compounds used in the plastic industry and consumer
products, and other industrial by-products and
pollutants (Damstra et al., 2002). Common EDCs
include phthalate acid esters, DDT, DDE, PCBs,
dioxins, and tributyl tin (Damstra et al., 2002). These
chemicals can exert profound and adverse effects on
aquatic animals by interfering with the endocrine
system and potentially resulting in reduced fertility
and population declines. The environment chemistry
of different EDCs is complex, the toxicity of
congeners can vary tremendously, and the analysis
is costly.
Many rubbers and plastics are toxic to phyto-
plankton, copepods, and other small marine organisms
(Bernhard, 1973), at least initially. Leaching for 10–30
days, may remove the toxicity from epoxy paints and
PVC components (Beaumont and Tserpes, 1984;
Carmignai and Bennett, 1976). Some plastic liners
have shown serious and long-term toxicity to fish,
shrimp, and nitrifying bacteria (Horowitz et al., 2001;
Zitko et al., 1985) and must not be used aquatic
systems. The heavy use of plastic and fiberglass in
reuse systems is likely to result in higher levels of
some EDCs and other trace contaminates compared to
flow-through and ponds systems. The toxicity of
plastic components is likely to be due to additives
(plasticizers, release agents, flame retardants, fungi-
cides, etc.) rather than the polymer itself. The
production of commodity plastics is an extremely
competitive business and a manufacturers may change
the brand or type of additives depending on costs
or other factors. Therefore, the toxicity of given
components from a single manufacturer may vary
significantly between production batches.
The use of ozone and activated carbon has shown
promise for removing EDCs from domestic waste-
water. Maturation and early rearing work with
sensitive species in reuse systems should pay special
attention to EDC and trace contaminate concerns.
5.5. Oxygen
The dissolved oxygen requirements of cool and
coldwater fishes have been reviewed by Davis (1975).
Generally, the dissolved oxygen should be maintained
above 5–6 mg/L except for channel catfish, guppy, or
eel where 3.0–3.5 mg/L is acceptable.
With the wide use of pure oxygen systems, the
impacts of supersaturated dissolved oxygen levels
must be considered. It is important to distinguish
between normbaric hyperoxia (elevated oxygen levels
at atmospheric pressure) and hyperbaric hyperoxia
(elevated oxygen levels at total pressures greater than
atmospheric pressure). Both types of hyperoxia can be
produced by different types of pure oxygen aeration. A
number of studies in the literature have confounded
J. Colt / Aquacultural Engineering 34 (2006) 143–156152
high DO concentrations and elevated total gas
pressure.
While oxygen is required for the survival of aerobic
organisms such as fish, some of the by-products of
oxygen metabolism are highly toxic and oxygen
toxicity may result (Fridovich, 1977). Highly active
and excitable fish such as striped bass Morone saxatilis
may be more susceptible to oxygen toxicity than less
active fish, although specific information on this
problem is lacking. Very high levels of dissolved
oxygen (>25 mg/L) should be avoided, especially for
eggs and small larvae.
When fish are acclimated to hyperoxia conditions,
ventilation rate decreases and respiratory carbon
dioxide gas is retained, resulting in a decrease in
blood pH. To compensate for this respiratory acidosis,
bicarbonate ion is retained by the kidneys to bring the
pH back to normal (Wood, 1991). This process of
compensation may take several days. If these fish are
suddenly transferred back to normal oxygen condi-
tions, the ventilation rate returns to normal and the
excess carbon dioxide gas can be unloaded from tissue
and blood in less than 30–60 min. This loss of carbon
dioxide can result in metabolic alkalosis and rapid
changes in blood pH. There are anecdotal reports of
fish mortality following rapid reduction in DO levels
but documentation is lacking in the literature.
Potential mortality could occur: (1) after failure of
oxygen supplementation systems, (2) upon transfer/
planting of fish from a facility using pure oxygen
supplementation, or (3) following 12–24 h of transport
under high dissolved oxygen concentrations.
High dissolved oxygen concentrations (>500
mmHg) can have significant developmental effects
on eggs and larvae (Gulidov, 1969). Commercial
salmon facilities in the Pacific Northwest routinely
used pure oxygen to increase the influent oxygen gas
pressures to 230–310 mmHg (Gowan, 1987).
5.6. Carbon dioxide
On a short-term basis, freshwater fish can withstand
greater than 100–200 mg/L of carbon dioxide (Basu,
1959). In work with rainbow trout, Smart et al. (1979)
found a 50% reduction in growth at approximately
60 mg/L. Growth reduction appears to be linearly
related to the carbon dioxide concentration. High
carbon dioxide concentrations results in the formation
of calcareous deposits in the kidney (nephrocalcino-
sis). In rainbow trout, increasing kidney damage was
observed above 24 mg/L, but only after 275 days of
exposure. Little information is available on the
impacts of carbon dioxide on warm water fish such
as catfish or tilapia, although it is generally assumed
that these fish are more tolerant of carbon dioxide
exposures.
Recent work with Atlantic salmon (Salmo salar)
has shown increased incidences of nephrocalcinosis at
16 and 24 mg/L carbon dioxide after 58 days exposure
(Fivelstad et al., 2003a). Nephrocalcinosis was also
observed in the control exposures held in 6 mg/L of
carbon dioxide, but the clinical signs of nephrocalci-
nosis for all exposure levels disappeared after transfer
to seawater. Freshwater exposure to carbon dioxide
affected tissue mineral content after the fish were
transferred to seawater.
Depending on the alkalinity, respiratory carbon
dioxide can depress the pH and mole fraction of
ammonia, resulting in very low concentrations of un-
ionized ammonia for relatively high TAN levels
(Colt and Orwicz, 1991). The decrease in toxicity of
un-ionized ammonia with decreasing pH must be
balanced against the increasing concentration of
carbon dioxide for a given total carbonate concen-
tration (CT). For water with very low pH and
alkalinity, the impacts of reduced pH on aluminum
deposition on the gills can be important (Fivelstad
et al., 2003b).
Water quality criteria for carbon dioxide cannot be
made at this time, especially for warmwater species.
While more is known about the impact of carbon
dioxide on coldwater species, potential impacts will
depend strongly on ambient water characteristics and
the severity of nephrocalcinosis that can be tolerated.
5.7. Heavy metals
In water reuse systems, the most important heavy
metals are cadmium, copper, and zinc. The source of
these metals can be corrosion of pipes and fittings or
metals added to feed as part of the vitamin premix. In
reuse systems with low make-up flows, there is a
potential to build-up toxic concentrations of copper
and zinc. The toxicity of heavy metals depends
strongly on water chemistry and is commonly reduced
at high alkalinities and hardness.
J. Colt / Aquacultural Engineering 34 (2006) 143–156 153
Chronic criteria (CCC) are presented below in
terms of dissolved heavy metals in mg/L based on
current USEPA water quality criteria (USEPA,
2002):
Metal
Freshwater Seawater500a
100a 10a 1aCopper
35 9 1.3 0.18 3.1Zinc
460 120 17 2.4 81Cadmium
0.75 0.25 0.049 0.01 8.8a Hardness (mg/L as CaCO3).
These criteria should be treated more as ‘‘action
levels’’ that true no-effects chronic criteria as the CCC
is based on reoccurrence interval of only once every 3
years. In addition, the impact of hardness on CCC is
based on waters with typical carbonate chemistry and
alkalinity–pH relationships. The functional relation-
ship between hardness and CCC may be different in a
high-intensity reuse system with a modified ionic
composition.
5.8. Fine solids
The greatest water quality uncertainty in high
intensity reuse systems is the potential impacts of fine
solids and organic compounds. Fish are resistant to
high levels of inorganic solids such as soil, clay, and
volcanic ash (Redding et al., 1987) but the buildup of
fine solids occurs in reuse systems (Chen et al., 1993;
Patternson and Watts, 2003a,b) and have been
implicated in disease outbreaks (Bullock et al.,
1994). Quantitative information on the impacts of
specific size fractions of fecal solids and uneaten feed
on growth and fish health is lacking.
5.9. Surface-active compounds
The leaching of surface-active compounds from
uneaten feed and fecal matter and its resulting
depression of surface tension may be an important
design consideration. These compounds may also
serve as substrate for bacteria and other micro-
organisms (Kindschi and MacConnell, 1989). The
adhesion and growth of marine bacteria has been
found to depend on surface tension (ZoBell, 1972),
and therefore, potentially have a direct impact on
development of some diseases. Surface tension is
relatively easy to measure (Lyklema, 2000) and may
be an important control parameter for reuse systems.
The leaching of oils from feeds and formation of
surface oil films may be a special problem in the
culture of small larvae.
5.10. Color compounds
The development of brown water in reuse systems
is common and assumed to be due to the accumula-
tion of humic acid compounds (Bovendeur et al.,
1987). Humic and fulvic acids are generally derived
from vascular plant matter and differ essentially in
the amount of biodegradation that occurs within the
soil (Ertel et al., 1986). Recent work has demon-
strated that formation of these color compounds
appears to depend on the content of processed fish
meal (Schuster, 1994). Isonitrogenous feeds using
minced fish instead of fish meal showed no increase
in color formation. Christensen et al. (2000)
developed a model to assist in the sizing of an
ozone contact system to remove color compounds
from a pilot-scale reuse system. The primary reason
for color removal in this study was to allow better
observation of the culture animal. Ozone is
commonly used for this purpose in large recirculat-
ing marine aquariums.
The chemistry of aquatic humic and fulvic acids is
complex (Ertel et al., 1986) and in some natural
tropical waters, the pH may be controlled by humic
and fulvic acids instead of the carbonate system
(Furch, 1984). Detailed information on the potential
impact of these compounds is lacking, but it is
common to add commercially prepared humic acid
extracts in the breeding of neon tetra (Paracheirodeon
innesi) (Chapman et al., 1998).
Absorbance of light in the ultraviolet region (250–
254 nm) has been found to be related to the content of
dissolved organics. Ultraviolet absorbance can be
determined rapidly and automatically. This method
could be used to continuously monitor dissolved
organics in a culture system.
The following relationships (Mrkva, 1983; Toi and
Satomi, 1978) have been found for UV absorbance
dissolved organics:
TOC ðmg=LÞ ¼ �0:28þ 40:03A250
COD ðmg=LÞ ¼ 7:5þ 101A254
J. Colt / Aquacultural Engineering 34 (2006) 143–156154
where A250 is the absorbance of 250 nm light in 1 cm
path length cell and A254 is the absorbance of 254 nm
light in 1 cm path length cell.
6. Conclusions
The purpose of this paper is to document how water
quality criteria are developed and assess their use in
production reuse systems. Many of the published
water quality criteria are not appropriate for reuse
systems because they were developed for the
protection of a number of species and sizes. Because
of economic considerations, it may also be necessary
to define the impacts of critical parameters over a wide
range of growth and mortalities. It may not be possible
to provide a ‘‘no effects’’ levels for all water quality
parameters. The development of appropriate water
quality criteria will require production testing and
monitoring and the cooperation of biologist, engi-
neers, and fish culturists.
References
Alabaster, J.S., Lloyd, R., 1980. Water Quality Criteria for Fresh-
water Fish. Butterworths, London, England.
Barton, B.A., 1996. General biology of salmonids. In: Pennell, W.,
Barton, B.A. (Eds.), Principles of Salmonid Culture. Elsevier,
Amsterdam, pp. 29–95.
Basu, S.P., 1959. Active respiration of fish in relation to ambient
concentrations of oxygen and carbon dioxide. J. Fish. Res. Bd.
Can. 16, 175–212.
Beaumont, A.R., Tserpes, G., 1984. The effects on Mytilus edulis
larvae of toxins leaching from paints. Aquaculture 38, 365–
369.
Bernhard, M., 1973. Chemical contamination of culture media:
assessment, avoidance and control. In: Kinne, O. (Ed.), Mar-
ine Ecology, vol. III, Part 3. John Wiley & Sons, New York, pp.
1459–1499.
Bovendeur, J., Eding, E.H., Henken, A.M., 1987. Design and
performance of a water recirculation systems for high density
culture of African catfish, Clarias gariepinus (Burchel 1922).
Aquaculture 63, 329–353.
Bower, C.E., Bidwell, J.P., 1978. Ionization of ammonia in seawater:
effects of temperature, pH, and salinity. J. Fish. Res. Bd. Can. 35,
1012–1016.
Boyd, C.E., Tucker, C.S., 1998. Pond Aquaculture Water Quality
Management. Kluwer Academic Publishers, Boston.
Brownell, C.L., 1980a. Water quality requirements for first-feeding
in marine fish larvae. I. Ammonia, nitrite, and nitrate. J. Exp.
Mar. Biol. Ecol. 44, 269–283.
Brownell, C.L., 1980b. Water quality requirements for first-feeding
in marine fish larvae. II. pH, oxygen, and carbon dioxide. J. Exp.
Mar. Biol. Ecol. 44, 285–298.
Bullock, G., Herman, R., Heinen, J., Noble, A., Weber, A., Hankins,
J.A., 1994. Observations on the occurrence of bacterial gill
disease and amoeba gill infestation in rainbow trout cultured
in a water recirculation system. J. Aquat. Anim. Health 6, 310–
317.
Carmignai, G.M., Bennett, J.P., 1976. Leaching of plastics used in
closed aquaculture systems. Aquaculture 7, 89–91.
Chapman, F.A., Colle, D.E., Rottmann, R.W., Shireman, J.V., 1998.
Controlled spawning of the neon tetra. Prog. Fish-Cult. 60, 32–
37.
Chen, S., Timmons, M.B., Aneshansley, D.J., Bisogni Jr., J.J., 1993.
Suspended solids characteristics from recirculating aquaculture
systems and design implications. Aquaculture 112, 143–155.
Christensen, J.M., Rusch, K.A., Malone, R.F., 2000. Development of
a model for describing accumulation of color and subsequent
destruction by ozone in a freshwater recirculating aquaculture
system. J. World Aquacult. Soc. 31, 167–174.
Clesceri, L.S., Greenberg, A.E., Eaton, A.D., 1998. Standard Meth-
ods for the Examination of Water and Wastewater, 20th ed.
American Public Health Association, Washington, DC.
Colt, J., Orwicz, K., 1991. Modeling production capacity of aquatic
culture systems under freshwater conditions. Aquacult. Eng. 10,
1–29.
Colt, J., Tchobanoglous, G., 1978. Chronic exposure of channel
catfish, Ictalurus punctatus, to ammonia: effects on growth and
survival. Aquaculture 15, 353–372.
Committee on Methods [The Committee on Methods for Toxicity
Tests with Aquatic Organisms], 1975. Ecological Research
Series, EPA-660/3-75-009, U.S. Environmental Protection
Agency, U.S. Government Printing Office, Washington, DC.
Conte, F.H., 1988. Hatchery Manual for the White Sturgeon (Aci-
penser transmontanus Richardson): With Application to Other
North American Acipenseridae. University of California, Oak-
land, California.
Costa-Pierce, B.A., Rakocy, J.E. (Eds.), 1997. Tilapia Aquaculture
in the Americas. World Aquaculture Society, Baton Rouge,
Louisiana.
Damstra, T., Barlow, S., Bergman, A., Kavlock, R., van der Kraaak,
G., 2002. Global Assessment of the State-of-the-science of
Endocrine Disruptors. WHO/PCS/EDC/02.2, World Health
Organization. (http://www.who.int/ipcs/publications/new_issues/
endocrine_disruptors/en/).
Davis, J.C., 1975. Minimal dissolved oxygen requirements of
aquatic life with emphasis on Canadian species: a review. J.
Fish. Res. Bd. Can. 32, 2295–2332.
Ertel, J.R., Hedges, J.I., Devol, A.H., Richey, J.E., Ribeiro,
M.de.N.G., 1986. Dissolved humic substances of the Amazon
River system. Limnol. Oceanogr. 31, 739–754.
Fivelstad, S., Olsen, A.B., Asgard, T., Baeverfjord, G., Rasmussen,
T., Vindheim, T., Stefansson, S., 2003a. Long-term sublethal
effects of carbon dioxide on Atlantic salmon smolts (Salmo salar
L.): ion regulation, haematology, elemental composition,
nephrocalcinosis and growth parameters. Aquaculture 215,
301–319.
J. Colt / Aquacultural Engineering 34 (2006) 143–156 155
Fivelstad, S., Waagbø, R., Seitz, S.F., Hosfeld, A.C.D., Olsen, A.B.,
Stefansson, S., 2003b. A major water quality problem in smolt
farms: combined effects of carbon dioxide, reduced pH and
aluminum on Atlantic salmon (Salmo salar L.) smolts: physiol-
ogy and growth. Aquaculture 215, 339–357.
Frakes, T., Hoff Jr., F.H., 1982. Effects of high nitrate-N on the
growth and survival of juvenile and larval anemonefish, Amphi-
prion ocellaris. Aquaculture 29, 155–158.
Fridovich, I., 1977. Oxygen is toxic. BioScience 27, 462–466.
Furch, K., 1984. Water chemistry of the Amazon basin: the dis-
tribution of chemical elements among freshwaters. In: Sioli, H.
(Ed.), The Amazon—Limnology and Landscape Ecology of a
Mighty Tropical River and its Basin. Dr. W. Junk Publishers,
Dordrecht, pp. 167–199.
Gowan, R., 1987. Use of supplemental oxygen to rear chinook in
seawater. In: Papers on the Use of Supplemental Oxygen to
Increase Hatchery Rearing Capacity in the Pacific Northwest,
Bonneville Power Administration, Portland, Oregon, pp. 35–
39.
Gulidov, M.V., 1969. Embryonic development of pike [Esox lucius
L.] when incubated under different oxygen conditions. Probl.
Ichthyol. 9, 841–851.
Hampson, B.L., 1977. Relationship between total ammonia and free
ammonia in terrestrial and ocean waters. J. Cons. Int. Explor.
Mer. 37, 117–122.
Hansson, I., 1973. A new set of pH-scales and standard buffers for
sea water. Deep-Sea Res. 20, 479–491.
Hargreaves, J.A., Kucuk, S., 2001. Effects of diel un-ionized
ammonia fluctuation on juvenile hybrid striped bass, channel
catfish, and blue tilapia. Aquaculture 195, 163–181.
Horowitz, A., Samocha, T.M., Gandy, R.L., Horowitz, S., 2001.
Toxicity tests to assess the effect of a synthetic tank liner on
shrimp survival and nitrification in a recirculating superintensive
production system. Aquacult. Eng. 24, 91–105.
Khoo, K.H., Culberson, C.H., Bates, R.G., 1977. Thermodynamics
of the dissociation of ammonium ion in seawater from 5 to
40 8C. J. Sol. Chem. 6, 281–290.
Kindschi, G.A., MacConnell, E., 1989. Factors influencing early
mortality of walleye fry reared intensively. Prog. Fish-Cult. 51,
220–226.
Lewis Jr., W.M., Morris, D.P., 1986. Toxicity of nitrite to fish: a
review. Trans. Am. Fish. Soc. 115, 183–195.
Lyklema, J., 2000. Fundamentals of interface and colloid science.
Liquid–Fluid Interfaces, vol. III. Academic Press, New York.
Mayes, A.M., Alexander, H.C., Hopkins, D.L., 1986. Acute and
chronic toxicity of ammonia to freshwater fish: a site-specific
study. Environ. Toxicol. Chem. 5, 437–442.
McKee, J.E., Wolf, H.W. (Eds.), 1968. Water Quality Criteria,
second ed. Publication No. 3-A, State Water Resources Control
Board, Sacramento, California.
Meade, J.W., 1985. Allowable ammonia for fish culture. Prog. Fish-
Cult. 47, 135–145.
Messer, J.J., Ho, J., Grenney, W.J., 1984. Ionic strength correction
for extent of ammonia ionization in freshwater. Can. J. Fish.
Aquat. Sci. 41, 811–815.
Millero, F.J., 1986. The pH of estuarine waters. Limnol. Oceanogr.
31, 839–847.
Mrkva, M., 1983. Evaluation of correlations between absorbance at
254 nm and COD of river waters. Water Res. 17, 231–235.
Nickum, J.G., Stickney, R.R., 1993. Walleye. In: Stickney, R.R.
(Ed.), Culture of Nonsalmonid Freshwater Fishes. second ed.
CRC Press, Boca Raton, Florida, pp. 231–250.
Patternson, R.N., Watts, K.C., 2003a. Micro-particles in recirculat-
ing aquaculture systems: particle size analysis of culture water
from a commercial Atlantic salmon site. Aquacult. Eng. 28, 99–
113.
Patternson, R.N., Watts, K.C., 2003b. Micro-particles in recirculat-
ing aquaculture systems: microscopic examination of particles.
Aquacult. Eng. 28, 115–130.
Peltier, W., 1978. Methods for measuring the acute toxicity of
effluents to aquatic organisms. Environmental Monitoring,
EPA-600/4-78-012, U.S. Environmental Protection Agency,
U.S. Government Printing Office, Washington, DC, 52 pp.
Pierce, R.H., Weeks, J.M., Prappas, J.M., 1993. Nitrate toxicity to
five species of marine fish. J. World Aquacult. Soc. 24, 105–107.
Piper, R.G., McElwain, I.B., Orme, L.E., McCraren, J.P., Fowler,
L.G., Leonard, J.R., 1982. Fish Hatchery Management. U.S.
Fish and Wildlife Service, Washington, DC.
Poxton, M.G., Allouse, S.B., 1982. Water quality criteria for marine
fisheries. Aquacult. Eng. 1, 153–191.
Redding, J.M., Schreck, C.B., Everest, F.H., 1987. Physiological
effects on coho salmon and steelhead of exposure to suspended
solids. Trans. Am. Fish. Soc. 116, 737–744.
Schuster, C., 1994. The effect of fish meal content in trout food on
water colour in a closed recirculating aquaculture system.
Aquacult. Int. 2, 266–269.
Schwedler, T.E., Tucker, C.S., 1983. Empirical relationship between
percent methemoglobin in channel catfish and dissolved nitrite
and chloride in ponds. Trans. Am. Fish. Soc. 112, 117–119.
Sigma 1983. Summary of Water Quality Criteria for Salmonid
Hatcheries. SECL 8067, Sigma Environmental Consultants
Limited, Prepared for Canada Dept. Fisheries and Oceans.
Smart, G.R., Knox, D., Harrison, J.G., Ralph, J.A., Richards, R.H.,
Cowey, C.B., 1979. Nephrocalcinosis in rainbow trout Salmo
gairdneri Richardson; the effect of exposure to elevated CO2
concentrations. J. Fish Dis. 2, 279–289.
Smith, C.E., Piper, R.P., 1975. Lesions associated with chronic
exposure to ammonia. In: Ribelin, W.E., Migaki, G. (Eds.),
Pathology of Fishes. University of Wisconisn Press, Madison,
Wisconsin, pp. 497–514.
Solomon, D.J., 1977. A review of chemical communication in
freshwater fish. J. Fish Biol. 11, 363–376.
Stickney, R.R., 1993. Channel catfish. In: Stickney, R.R. (Ed.),Culture
of Nonsalmonid Freshwater Fishes. second ed. CRC Press, Boca
Raton, Florida, pp. 33–80.
Thurston, R.V., Russo, R.C., Luedtke, R.J., Smith, C.E., Meyn, E.L.,
Chakoumakos, C., Wang, K.C., Brown, C.J.D., 1984. Chronic
toxicity of ammonia to rainbow trout. Trans. Am. Fish. Soc. 113,
56–73.
Toi, J., Satomi, Y., 1978. Relations between ultraviolet absorbance
and dissolved organic matter in the fish culture pond water. Bull.
Freshwater Fish. Res. Lab. 28, 189–198.
Tomasso, J.R., 1994. Toxicity of nitrogenous wastes to aquaculture
animals. Rev. Fish. Sci. 2, 291–314.
J. Colt / Aquacultural Engineering 34 (2006) 143–156156
Tomasso, J.R., 1997. Environmental requirements and noninfectious
diseases. In: Harrell, R.M. (Ed.), Striped Bass and Other Morone
Culture. Elsevier, New York, pp. 253–270.
USEPA [U.S. Environmental Protection Agency], 1976. Water
Quality Criteria for Water. U.S. Environmental Protection
Agency, Washington, DC.
USEPA [U.S. Environmental Protection Agency], 1985. Guidelines
for Deriving Numerical National Aquatic Life Criteria for
Protection of Aquatic Organisms and Their Uses. U.S. Environ-
mental Protection Agency, Washington, DC. [www.epa.gov/
waterscience/criteria/aqlife.html].
USEPA [U.S. Environmental Protection Agency], 1986. Water
Quality Criteria for Water. U.S. Environmental Protection
Agency, Washington, DC. [www.epa.gov/waterscience/criteria/
goldbook.pdf].
USEPA [U.S. Environmental Protection Agency], 2002. National
Recommended Water Quality Criteria: 2002. Office of
Water, EPA-822-R-02-047, U.S. Environmental Protection
Agency, Washington, DC. [www.epa.gov/waterscience/standards/
wqcriteria. html].
Walsh, L.S., Turk, P.E., Lee, P.G., 2002. Mariculture of the loliginid
squid Sepioteuthis lessoniana through seven successive genera-
tions. Aquaculture 212, 245–262.
Wedemeyer, G.A., 1996. The Physiology of Fish in Intensive
Culture Systems. Chapman & Hall, New York, 272 pp.
Westers, H., 1981. Fish Culture Manual for the State of Michigan.
Michigan Department of Natural Resources, Lansing, Michigan.
Westers, H., Stickney, R.R., 1993. Northern Pike and Muskellunge. In:
Stickney, R.R. (Ed.), Culture of Nonsalmonid Freshwater Fishes.
second ed. CRC Press, Boca Raton, Florida, pp. 199–214.
Whitfield, M., 1978. The hydrolysis of ammonium ions in sea
water—experimental confirmation of predicted constants at
one atmosphere pressure. J. Mar. Biol. Ass. U.K. 58, 781–787.
Wickins, J.F., 1981. Water quality requirements for intensive aqua-
culture: a review. In: Tiews, K. (Ed.), Aquaculture in Heated
Effluents and Recirculation Systems, vol. 1. Heenemann Ver-
lagsgesellschaft, Berlin, pp. 17–37.
Williamson, J.H., Carmichael, G.J., Graves, K.G., Simco, B.A.,
Tomasso, J.R., 1993. Centrarchids. In: Stickney, R.R. (Ed.),
Culture of Nonsalmonid Freshwater Fishes. second ed. CRC
Press, Boca Raton, Florida, pp. 145–198.
Wood, C.M., 1991. Branchial ion and acid-base transfer in fresh-
water teleost fish: environmental hyperoxia as a probe. Physiol.
Zool. 64, 68–102.
Zitko, V., Burridge, L.E., Woodside, M., Jerome, V., 1985. Mor-
talities of juvenile Atlantic salmon caused by the fungicide
OBPA. Can. Tech. Rep. Fish. Aquat. Sci. 1358 29 pp.
ZoBell, C.E., 1972. Substratum. Bacteria, fungi and blue-green
algae. In: Kinne, O. (Ed.), Marine Ecology, vol. I, Part 3.
Wiley-Interscience, London, pp. 1251–1270.