You are on page 1of 14

Aquacultural Engineering 34 (2006) 143156 www.elsevier.

com/locate/aqua-online

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, ne 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 biolter operation are also needed. Published by Elsevier B.V.
Keywords: Water quality criteria; Reuse; Fine solids; Surface active compounds; Carbon dioxide

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 ow-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 specic 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: john.colt@noaa.gov. 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 signicant impact on overall production economics. In addition, the culture objectives (food production versus endangered species enhancement) may also change the specic 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-

144

J. Colt / Aquacultural Engineering 34 (2006) 143156

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 difcult 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-specic criteria may be developed.

aquatic organisms such as zebra sh (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 signicance using common statistical tests and three specic parameters are commonly reported in toxicity literature (Mayes et al., 1986):  The no-observable-effects concentration (NOEC): The high concentration tested at which some selected effect failed to be produced within some specied period of exposure.  The lowest-observable-effect concentration (LOEC): The lowest concentration at which a selected effect is observed.  The 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 signicance 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 elds.

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 sh 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 difcult to conduct because of complexity of experimental controls and the statistical need for replication. Some acute toxicity experiments are relatively short-term (2496 h) but sublethal exposure trials commonly require 3090+ 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 lifecycle toxicity test of ammonia to any sh 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 denes partial life cycle and early lifestage experiments (USEPA, 1985). Because of the difculty of working with long-generation time species (and most commercially important species), there is an increasing tendency to work with smaller

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 periodically update ambient water quality criteria. Water quality criteria developed under Section 304(a) are based solely on data and scientic judgments on the relationship between pollutant concentrations and environmental and human health effects. Section 304(a) criteria do not reect 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 consumption of sport caught sh and invertebrates while the U.S. Food and Drug Agency (FDA) regulates

J. Colt / Aquacultural Engineering 34 (2006) 143156

145

commercially marketed sh and seafood products. The action levels and recommended consumption levels are signicantly 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 10100. 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 developed: 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 scientic 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 water reuse applications The selection of water quality criteria for water reuse may be based on published environmental protection criteria, species-specic publications, or aquaculture books, or may require development of site and species-specic criteria. The selection of criteria depends strongly on the species reared, culture objectives, and regulatory requirements. Basic information 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 1020 cm tilapia or rainbow trout. The impact of a parameter on broodstock, eggs,

146

J. Colt / Aquacultural Engineering 34 (2006) 143156

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 300400 g channel catsh 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 difcult 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 documentation on the impacts of xed and variable ammonia concentrations on ngerling channel catsh (110 g) (Colt and Tchobanoglous, 1978; Hargreaves and Kucuk, 2001), there is little documentation for larger sh (>20400 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 ngerlings and larger sh. 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 specic 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 appropriate. 4.2. Fisheries and aquaculture and books Species handbooks, sh 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 Salmonids Temperate basses Channel catsh Black basses Sunshes Walleye Pikes Tilapia Sturgeon Marine sh Marine larval shes General Reference Barton (1996), Piper et al. (1982), Sigma (1983), Wedemeyer (1996) Tomasso (1997) Boyd and Tucker (1998), Stickney (1993) Williamson et al. (1993) Williamson et al. (1993) Nickum and Stickney (1993) Westers and Stickney (1993) Costa-Pierce and Rakocy (1997) Conte (1988) Poxton and Allouse (1982) Brownell (1980a,b) Wickins (1981)

While these sources are very useful, it is important to realize that in general, they will depend on primary data with the same limitation as discussed previously. Commonly, much of information contained in these sources is based on the experiences and practices of state, tribal, and federal hatchery programs. Current information from largescale commercial enterprises is very difcult to nd.

J. Colt / Aquacultural Engineering 34 (2006) 143156 Table 1 Important factors in the selection of water quality criteria for aquatic culture systems Type of criteria Lethal effects Sublethal effects Growth Fin quality and appearance Tissue quality Physiological quality Behavioral and sh health quality Endocrine, reproductive, or immune impacts in animals and humans Regulatory requirements Phosphorous, nitrogenous compounds, BOD, suspended solids, and chemical releases Trace contaminates in tissue Disease causing microorganisms Example

147

Important in the design of backup systems, transport systems, and holding system at processing plants Basic parameter in production systems Importance for products sold alive and for some products consumed in a specic manner Product quality (texture, taste, and odor) for human consumption Smoltication in anadromous salmonids Ability of stocked animals to adapt and survive after planting (enhancement and restoration) Caused by endocrine disrupters (environmental estrogens or estrogenic xenobiotics) Efuent discharge requirements under the Clean Water Act Levels of methymercury, PCB, DDT, or dioxins may limit human consumption (amount or frequency) Hepatitis A, Vibrio spp., E. coli

4.3. Development of facility specic 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 specic 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 tted to many growth studies:

where m is the slope of the growth curve; a, b, c are the regression coefcients; Y is the value of the specic parameter. Assuming that growth information is available, is it relatively simple to compute the selected regression curves with commonly available statistical or graphing programs, but selection of the appropriate value of Y will still require judgment and perhaps validation. The physiological and behavioral quality of sh may be more important if sh are to be released to nature. The design of backup water or aeration systems, transport systems, or holding vats at processing plants may be designed to prevent signicant 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

Growth rate % of maximum 100 m Y Growth rate % of maximum 100 a Y b Y 2 Growth rate % of maximum 100 a Y b Y 2 c Y 3

linear second order polynominal third order polynominal

148

J. Colt / Aquacultural Engineering 34 (2006) 143156

technology (better feeds, pure oxygen, ozone disinfection, 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 eld verication. Meade (1985) concluded that a truly safe, maximum acceptable concentration of unionized, or total, ammonia for sh 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. Estimate maximum or safe concentrations based on available information. 2. Develop production indexes based on holistic data collected by monitoring a number of rearing systems.

3. Adjust safe concentrations based on monitor information and validate with additional monitoring. Development of species or system specic water quality criteria is time consuming, expensive, and may be difcult to publish in a peer-reviewed journal. A summary of important water quality parameters is presented in Table 2. Each parameter is classied 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 xed criterion, a variable criterion, or an indicator criterion. A variable criterion is needed for parameters that have signicant 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

Table 2 Chemical and physical parameters important to culture animals and/or discharge in aquatic systems Type Metabolic wastes Parameter Ammonia Nitrite Nitrate Pheromones Fecal wastes (large solids) Fine solids Oxygen Carbon dioxide Hydrogen sulde Gas supersaturation Heavy metals Chlorine Ozone Biocides, toxic organics Salinity/total dissolved solids Solids/turbidity pH P compounds Surface-active compounds Color compounds Yes Cost implications Yes Yes Type of criteriaa V, I V, I A ? A V V V A A A A A A A A A A I I H H Priority in reuse H H H H H H H

Yes Yes Yes Yes

Dissolved gases

Toxics

Dissolved or suspended material

Nutrients Other parameters


a

A, xed criterion; V, variable criterion; I, indicator criterion.

J. Colt / Aquacultural Engineering 34 (2006) 143156 Table 3 Chemical and physical parameters important to biolter operations Parameter Nitrate Oxygen Therapeutic drugs and chemicals pH (and alkalinity) Salinity Implications

149

A minimum level of nitrate will prevent formation of hydrogen sulde in ponds subjected to anaerobic conditions Nitrication stops at low dissolved oxygen Drugs and chemicals can have a serious impact on nitrication The nitrication process slows down at high and low pHs Different bacteria are responsible for nitrication in freshwater and seawater. Rapid changes in salinity can reduce the rate of nitrication for a period of time

implications, it may be possible to select a single xed 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 inuent 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 biolter performance that may adversely inuence a number of other water quality parameters that are more difcult (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 biolter 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 biolter operation (Table 3). Detailed information will be presented on these parameters in other articles in this special issue.

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 sh has been reviewed by Tomasso (1994). The toxicity of ammonia is generally assumed to be due to the concentration of the un-ionized ammonia molecule (NH3) because of its ability to move across cell membranes. The concentration of NH3 can be computed from the following equation: NH3 N TAN 1 10pKa pH

5. Critical water quality parameters in reuse systems Compared to ow-through or ponds, reuse systems typically have signicantly reduced make-up ows 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

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 9.00 8.00 7.00 6.00 5.00 4.00 NH3 N (mg/L) 1430 191 20 2 0.2 0.02

150

J. Colt / Aquacultural Engineering 34 (2006) 143156

At a pH of 9.0 and TAN = 5 mg/L, typical sh 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 uctuations) 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 1020% 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 (Whiteld, 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 Whiteld (1978) or Khoo et al. (1977) can over-estimate the un-ionized ammonia concentration 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 catsh (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: HNO2 N TNN 1 10pHpKa

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 9.00 8.00 7.00 6.00 5.00 4.00 HNO2 N (mg/L) 0.0024 0.024 0.240 2.40 28 166

At 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 sh from the toxicity of nitrite by competitively excluding nitrite from uptake by the chloride active transport mechanism in the gills. In pond culture of channel catsh, 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) 143156

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 sh 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 undocumented nitrite levels. The nitrate-N concentrations should be less than 500 mg/L for large marine sh (Pierce et al., 1993), but marine tropical sh such as anemonesh (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 signicant role in many aspects of behavior and development such as homing of migratory sh, 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 sh species held in reuse systems, although documentation is currently lacking. Endocrine-disrupting chemicals (EDCs) encompass 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 phytoplankton, copepods, and other small marine organisms (Bernhard, 1973), at least initially. Leaching for 1030 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 sh, 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 berglass in reuse systems is likely to result in higher levels of some EDCs and other trace contaminates compared to ow-through and ponds systems. The toxicity of plastic components is likely to be due to additives (plasticizers, release agents, ame retardants, fungicides, 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 signicantly between production batches. The use of ozone and activated carbon has shown promise for removing EDCs from domestic wastewater. 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 shes have been reviewed by Davis (1975). Generally, the dissolved oxygen should be maintained above 56 mg/L except for channel catsh, guppy, or eel where 3.03.5 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

152

J. Colt / Aquacultural Engineering 34 (2006) 143156

high DO concentrations and elevated total gas pressure. While oxygen is required for the survival of aerobic organisms such as sh, some of the by-products of oxygen metabolism are highly toxic and oxygen toxicity may result (Fridovich, 1977). Highly active and excitable sh such as striped bass Morone saxatilis may be more susceptible to oxygen toxicity than less active sh, although specic 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 sh 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 sh are suddenly transferred back to normal oxygen conditions, the ventilation rate returns to normal and the excess carbon dioxide gas can be unloaded from tissue and blood in less than 3060 min. This loss of carbon dioxide can result in metabolic alkalosis and rapid changes in blood pH. There are anecdotal reports of sh 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 sh from a facility using pure oxygen supplementation, or (3) following 1224 h of transport under high dissolved oxygen concentrations. High dissolved oxygen concentrations (>500 mmHg) can have signicant developmental effects on eggs and larvae (Gulidov, 1969). Commercial salmon facilities in the Pacic Northwest routinely used pure oxygen to increase the inuent oxygen gas pressures to 230310 mmHg (Gowan, 1987). 5.6. Carbon dioxide On a short-term basis, freshwater sh can withstand greater than 100200 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 (nephrocalcinosis). 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 sh such as catsh or tilapia, although it is generally assumed that these sh 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 nephrocalcinosis for all exposure levels disappeared after transfer to seawater. Freshwater exposure to carbon dioxide affected tissue mineral content after the sh 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 unionized 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 concentration (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 ttings or metals added to feed as part of the vitamin premix. In reuse systems with low make-up ows, 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) 143156

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 500a Copper Zinc Cadmium
a

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 lms may be a special problem in the culture of small larvae. 5.10. Color compounds

Seawater 100a 9 120 0.25 10a 1.3 17 0.049 1a 0.18 2.4 0.01 3.1 81 8.8

35 460 0.75

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 alkalinitypH relationships. The functional relationship between hardness and CCC may be different in a high-intensity reuse system with a modied ionic composition. 5.8. Fine solids The greatest water quality uncertainty in high intensity reuse systems is the potential impacts of ne 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 ne 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 specic size fractions of fecal solids and uneaten feed on growth and sh 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 microorganisms (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

The development of brown water in reuse systems is common and assumed to be due to the accumulation 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 demonstrated that formation of these color compounds appears to depend on the content of processed sh meal (Schuster, 1994). Isonitrogenous feeds using minced sh instead of sh 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 recirculating 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 mg=L 0:28 40:03A250 COD mg=L 7:5 101A254

154

J. Colt / Aquacultural Engineering 34 (2006) 143156 Brownell, C.L., 1980b. Water quality requirements for rst-feeding in marine sh larvae. II. pH, oxygen, and carbon dioxide. J. Exp. Mar. Biol. Ecol. 44, 285298. 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, 8991. 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, 143155. 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, 167174. Clesceri, L.S., Greenberg, A.E., Eaton, A.D., 1998. Standard Methods 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, 129. Colt, J., Tchobanoglous, G., 1978. Chronic exposure of channel catsh, Ictalurus punctatus, to ammonia: effects on growth and survival. Aquaculture 15, 353372. 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 Ofce, Washington, DC. Conte, F.H., 1988. Hatchery Manual for the White Sturgeon (Acipenser transmontanus Richardson): With Application to Other North American Acipenseridae. University of California, Oakland, 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, 22952332. 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, 739754. sga rd, T., Baeverfjord, G., Rasmussen, Fivelstad, S., Olsen, A.B., A 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, 301319.

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 dene 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, engineers, and sh culturists.

References
Alabaster, J.S., Lloyd, R., 1980. Water Quality Criteria for Freshwater 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. 2995. Basu, S.P., 1959. Active respiration of sh in relation to ambient concentrations of oxygen and carbon dioxide. J. Fish. Res. Bd. Can. 16, 175212. 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.), Marine Ecology, vol. III, Part 3. John Wiley & Sons, New York, pp. 14591499. Bovendeur, J., Eding, E.H., Henken, A.M., 1987. Design and performance of a water recirculation systems for high density culture of African catsh, Clarias gariepinus (Burchel 1922). Aquaculture 63, 329353. Bower, C.E., Bidwell, J.P., 1978. Ionization of ammonia in seawater: effects of temperature, pH, and salinity. J. Fish. Res. Bd. Can. 35, 10121016. Boyd, C.E., Tucker, C.S., 1998. Pond Aquaculture Water Quality Management. Kluwer Academic Publishers, Boston. Brownell, C.L., 1980a. Water quality requirements for rst-feeding in marine sh larvae. I. Ammonia, nitrite, and nitrate. J. Exp. Mar. Biol. Ecol. 44, 269283.

J. Colt / Aquacultural Engineering 34 (2006) 143156 Fivelstad, S., Waagb, 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: physiology and growth. Aquaculture 215, 339357. Frakes, T., Hoff Jr., F.H., 1982. Effects of high nitrate-N on the growth and survival of juvenile and larval anemonesh, Amphiprion ocellaris. Aquaculture 29, 155158. Fridovich, I., 1977. Oxygen is toxic. BioScience 27, 462466. Furch, K., 1984. Water chemistry of the Amazon basin: the distribution of chemical elements among freshwaters. In: Sioli, H. (Ed.), The AmazonLimnology and Landscape Ecology of a Mighty Tropical River and its Basin. Dr. W. Junk Publishers, Dordrecht, pp. 167199. 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 Pacic 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, 841851. Hampson, B.L., 1977. Relationship between total ammonia and free ammonia in terrestrial and ocean waters. J. Cons. Int. Explor. Mer. 37, 117122. Hansson, I., 1973. A new set of pH-scales and standard buffers for sea water. Deep-Sea Res. 20, 479491. Hargreaves, J.A., Kucuk, S., 2001. Effects of diel un-ionized ammonia uctuation on juvenile hybrid striped bass, channel catsh, and blue tilapia. Aquaculture 195, 163181. 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 nitrication in a recirculating superintensive production system. Aquacult. Eng. 24, 91105. 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, 281290. Kindschi, G.A., MacConnell, E., 1989. Factors inuencing early mortality of walleye fry reared intensively. Prog. Fish-Cult. 51, 220226. Lewis Jr., W.M., Morris, D.P., 1986. Toxicity of nitrite to sh: a review. Trans. Am. Fish. Soc. 115, 183195. Lyklema, J., 2000. Fundamentals of interface and colloid science. LiquidFluid 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 sh: a site-specic study. Environ. Toxicol. Chem. 5, 437442. 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 sh culture. Prog. FishCult. 47, 135145. 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, 811815. Millero, F.J., 1986. The pH of estuarine waters. Limnol. Oceanogr. 31, 839847.

155

Mrkva, M., 1983. Evaluation of correlations between absorbance at 254 nm and COD of river waters. Water Res. 17, 231235. 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. 231250. Patternson, R.N., Watts, K.C., 2003a. Micro-particles in recirculating 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 recirculating aquaculture systems: microscopic examination of particles. Aquacult. Eng. 28, 115130. Peltier, W., 1978. Methods for measuring the acute toxicity of efuents to aquatic organisms. Environmental Monitoring, EPA-600/4-78-012, U.S. Environmental Protection Agency, U.S. Government Printing Ofce, Washington, DC, 52 pp. Pierce, R.H., Weeks, J.M., Prappas, J.M., 1993. Nitrate toxicity to ve species of marine sh. J. World Aquacult. Soc. 24, 105107. 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 sheries. Aquacult. Eng. 1, 153191. 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, 737744. Schuster, C., 1994. The effect of sh meal content in trout food on water colour in a closed recirculating aquaculture system. Aquacult. Int. 2, 266269. Schwedler, T.E., Tucker, C.S., 1983. Empirical relationship between percent methemoglobin in channel catsh and dissolved nitrite and chloride in ponds. Trans. Am. Fish. Soc. 112, 117119. 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, 279289. 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. 497514. Solomon, D.J., 1977. A review of chemical communication in freshwater sh. J. Fish Biol. 11, 363376. Stickney, R.R., 1993. Channel catsh. In: Stickney, R.R. (Ed.), Culture of Nonsalmonid Freshwater Fishes. second ed. CRC Press, Boca Raton, Florida, pp. 3380. 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, 5673. Toi, J., Satomi, Y., 1978. Relations between ultraviolet absorbance and dissolved organic matter in the sh culture pond water. Bull. Freshwater Fish. Res. Lab. 28, 189198. Tomasso, J.R., 1994. Toxicity of nitrogenous wastes to aquaculture animals. Rev. Fish. Sci. 2, 291314.

156

J. Colt / Aquacultural Engineering 34 (2006) 143156 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. 199214. Whiteld, M., 1978. The hydrolysis of ammonium ions in sea waterexperimental conrmation of predicted constants at one atmosphere pressure. J. Mar. Biol. Ass. U.K. 58, 781787. Wickins, J.F., 1981. Water quality requirements for intensive aquaculture: a review. In: Tiews, K. (Ed.), Aquaculture in Heated Efuents and Recirculation Systems, vol. 1. Heenemann Verlagsgesellschaft, Berlin, pp. 1737. 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. 145198. Wood, C.M., 1991. Branchial ion and acid-base transfer in freshwater teleost sh: environmental hyperoxia as a probe. Physiol. Zool. 64, 68102. Zitko, V., Burridge, L.E., Woodside, M., Jerome, V., 1985. Mortalities 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. 12511270.

Tomasso, J.R., 1997. Environmental requirements and noninfectious diseases. In: Harrell, R.M. (Ed.), Striped Bass and Other Morone Culture. Elsevier, New York, pp. 253270. 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. Environmental 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. Ofce 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 generations. Aquaculture 212, 245262. Wedemeyer, G.A., 1996. The Physiology of Fish in Intensive Culture Systems. Chapman & Hall, New York, 272 pp.

You might also like