Nitrogen biogeochemistry of aquaculture ponds

Aquaculture 166 Ž1998. 181–212 Review Nitrogen biogeochemistry of aquaculture ponds 1 John A. Hargreaves Mississippi State UniÕersity, Department of Wildlife and Fisheries, Box 9690, Mississippi State, MS 39762, USA Accepted 6 June 1998 Abstract Nitrogen ŽN. biogeochemistry of aquaculture ponds is dominated by biological transformations of N added to ponds in the form of inorganic or organic fertilizers and formulated feeds. Nitrogen application in excess of pond assimilatory capacity can lead to the deterioration of water quality through the accumulation of nitrogenous compounds Že.g., ammonia and nitrite. with toxicity to fish or shrimp. Principal sources of ammonia include fish excretion and sediment flux derived from the mineralization of organic matter and molecular diffusion from reduced sediment, although cyanobacterial nitrogen fixation and atmospheric deposition are occasionally important. Principal sinks for ammonia include phytoplankton uptake and nitrification. The magnitude of losses by ammonia volatilization and ammonium fixation to cation exchange sites is minor, but unknown. Interactions between pond sediment and water are important regulators of N biogeochemistry. Sediment represents a source of ammonia and a sink for nitrite and nitrate. The large volume of reduced sediment suggests that the potential for N removal by denitrification is high, although the magnitude of N removal by this mechanism is low because nitrification and denitrification are tightly coupled in aquatic sediments and sediment nitrification is limited by the depth of sediment oxygen penetration. Nitrogen biogeochemistry of aquaculture ponds is affected by feeds and feeding practices, water exchange and circulation, aeration, pond depth and other management procedures. Opportunities for management of N biogeochemistry are limited and goals are based largely on the intensity of fish production. q 1998 Published by Elsevier Science B.V. All rights reserved. Keywords: Ammonia; Nitrification; Denitrification; Sediment 1 Approved for publication as Journal Article No. J-9356 of the Mississippi Agricultural and Forestry Experiment Station, Mississippi State University. 0044-8486r98r$19.00 q 1998 Published by Elsevier Science B.V. All rights reserved. PII S 0 0 4 4 - 8 4 8 6 Ž 9 8 . 0 0 2 9 8 - 1 182 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 1. Importance of nitrogen in pond culture systems The efficiency of fish nitrogen ŽN. assimilation has important implications for water quality and profitability of pond aquaculture. Results from a variety of culture systems indicate that, on average, about 25% Žrange: 11 to 36%. of N added as feed or other nutrient input is recovered by the target organism ŽTable 1.. Protein sources such as fish meal and soybean meal are the most expensive components of formulated feeds and improvement in the efficiency of N assimilation and utilization will thus improve the economics of fish production. The inherent efficiency of nutrient utilization by fish implies that N loading of aquaculture ponds may be limited by the capacity to assimilate nitrogenous excretion, which may have a deleterious impact on water quality and fish growth. Following dissolved oxygen, the accumulation of dissolved inorganic nitrogen ŽDIN. is the factor most likely to limit feeding rate in aquaculture ponds ŽKnud-Hansen et al., 1991b.. Ammonia 2 is excreted as the end product of protein catabolism, and may be toxic if allowed to accumulate. Ammonia toxicity is manifest by hyperactivity, convulsions, loss of equilibrium, lethargy and coma. However, ammonia toxicity in aquaculture ponds is most likely expressed as the sublethal reduction of fish growth or suppression of immunocompetence, rather than as acute toxicity leading to mortality. Colt and Tchobanoglous Ž1978. demonstrated linear reduction of channel catfish growth over the range 0.05 to 1.0 mg ly1 NH 3 –N and a calculated 50% reduction of growth at about 0.5 mg ly1 NH 3 –N. The mechanisms of ammonia toxicity have not been firmly established. However, a combination of plasma sodium depletion ŽColt and Tchobanoglous, 1978; Tomasso et al., 1980., biochemical effects of Krebs cycle suppression by depletion of a-ketoglutarate ŽSousa and Meade, 1977; Smart, 1978. resulting in reduced ammonia excretion, and other factors ŽMeade, 1985. are implicated. The toxicity of un-ionized ammonia is a function of pH, temperature, alkalinity and total ammonia concentration measured at the gill surface ŽSzumski et al., 1982.. Ammonia is more toxic to fish at elevated pH and temperature, which shifts the ionization equilibrium toward the toxic, unionized gaseous form. The risk of elevated pH and unionized ammonia is greater in poorly buffered Žlow alkalinity. ponds in the late afternoon. The contribution of ammonia excretion to N flow in aquaculture ponds is substantial. If 25% of input N is retained by fish, then 75% of input N is excreted. Nitrogen excretion can be partitioned into dissolved Ž62%. and particulate Ž13%. fractions ŽFolke and Kautsky, 1989.. For example, at a feeding rate of 100 kg hay1 dy1 Ž32% protein feed., ammonia excretion would be 317 mg N my2 dy1. Alternately, using a feed-based estimate of ammonia excretion of 30 g N kgy1 feed ŽColt and Orwicz, 1991., then 300 mg N my2 dy1 are excreted. 2 Ammonia exists as a component of a pH- and temperature-dependent equilibrium in natural waters. Across the range of pH most commonly encountered in natural waters Ž6.5 to 9.0., the equilibrium favors the . Ž . aqueous, ionized form ŽNHq 4 , or ‘ammonium’. Elevated pH )9.3 favors the gaseous, unionized form ŽNH 3 ., or ‘ammonia’. The convention adopted here will be to use the term ‘ammonia’ to refer to unionized . expressed as nitrogen by mass unless otherwise explicitly ammonia plus ionized ammonium ŽNH 3 q NHq 4 indicated. J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 183 Table 1 Estimates of the range Ž%. of nitrogen recovered by fish and released to the environment in various aquaculture production systems Fish species Production Recovered Released Refs. systema Fish Total Dissolved Solid polyculture Anguilla japonica Oreochromis niloticus Oreochromis spp. Morone saxatilis Ictalurus punctatus Sparus aurata S. aurata S. aurata S. aurata Oncorhynchus mykiss O. mykiss O. mykiss Salmo salar Salmo salar Clarias macrocephalus I. punctatus O. mykiss P P P P P P P P T T C C C C C C R R a 11–16 14–25 18–21 25–29 22 27 36 26 27 30 21 25 25–29 25 25 24 14 19 84–89 75–86 79–82 75–81 78 73 64 74 66 60 49 60 7 10 30 15 62 65 13 10 74 7 71–75 76 86 Schroeder et al., 1990 Chiba, 1986 Green and Boyd, 1995 Avnimelech and Lacher, 1979 Daniels and Boyd, 1989 Boyd, 1985 Krom et al., 1985 Neori and Krom, 1991 Neori and Krom, 1991 Porter et al., 1987 Phillips and Beveridge, 1986 Pillay, 1992 Penczak et al., 1982 Folke and Kautsky, 1989 Gowen and Bradbury, 1987 Lin et al., 1993 Worsham, 1975 Foy and Rosell, 1991a,b Production system codes: P searthen pond, T s tank, C s cage, R s raceway. Fish also excrete fecal solid wastes that settle to the sediment along with senescent phytoplankton and other particulate organic matter. By the mass balance approach Ž13% N as particulate solids., then 67 mg N my2 dy1 are excreted as fecal solids at a feeding rate of 100 kg hay1 dy1 . Alternately, fecal solids can account for up to 50% by weight of dry weight feed applied to the pond ŽColt and Orwicz, 1991.. Feces from catfish fed a 32% protein feed are 13.1% protein ŽBrown et al., 1989.. By this analysis, fecal solids contribute 104 mg N my2 dy1 . A large fraction of this organic matter is rapidly hydrolyzed and mineralized, representing an additional source of ammonia. Nitrite is another potentially-toxic nitrogenous compound that may accumulate in fish culture ponds. Nitrite is released as an intermediate product during nitrification and denitrification. The toxicity of nitrite is expressed through the competitive binding of nitrite to hemoglobin forming methemoglobin, which does not have the capacity to carry oxygen. Nitrogen may limit the primary productivity of ponds in which fish yields are dependent upon the development of autotrophic food webs. Thus, organic and inorganic fertilization programs may be directed toward increasing the availability of N for phytoplankton ŽNoriega-Curtis, 1979; Green et al., 1989; Schroeder et al., 1990; Knud-Hansen et al., 1991a,b.. Nitrogen discharged in fish pond effluents may degrade the quality of receiving waters. Given the inherent nutrient utilization efficiency described above, large quantities of nutrients may be released to the environment. Compared to concentrations in 184 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 influent water, Ziemann et al. Ž1992. measured an increase of total N and ammonia and a decrease of nitrate in the effluent from freshwater fish and prawn ponds and marine fish and shrimp ponds. Similarly, Tucker and Lloyd Ž1985a. measured higher concentrations of total N and ammonia and lower concentrations of nitrate in channel catfish ponds as compared to nearby receiving streams. Most of the N discharged from fish ponds is associated with algal and detrital biomass. In general, the discharge of N to the environment from ponds is comparatively lower than that from raceways and cages. Schwartz and Boyd Ž1994. measured the quantities of nutrients discharged during the draining and harvest of three channel catfish ponds and calculated that 18.6 g N kgy1 fish were released to the environment. The discharge of N from shrimp ponds is variable and depends upon water exchange rate. Estimates of the quantity of N discharged from shrimp ponds range from 17 to 58 g N kgy1 shrimp ŽSmith, 1995. to 102 " 25 g N kgy1 shrimp ŽBriggs and Funge-Smith, 1994.. In contrast, from 37 to 180 g N kgy1 rainbow trout were discharged from raceways ŽAlabaster, 1982. and from 95 to 102 g N kgy1 rainbow trout were discharged from cages ŽHall et al., 1992.. 2. Processes related to nitrogen flux in aquaculture ponds 2.1. Feeding and fertilization Application of formulated feeds constitutes the main Ž) 90%. input of N to semi-intensive fish ponds. For example, at a feeding rate of 100 kg hay1 dy1 Ž10 g my2 dy1 . of 32% protein feed, more than 500 mg N my2 dy1 are added to ponds. Organic and inorganic fertilizers may also supply significant quantities of N to fish ponds. In systems managed for autotrophic productivity, a net fish yield of 30 to 40 kg hay1 dy1 Ž3 to 4 g my2 dy1 . is possible at a loading of 700 to 800 mg N my2 dy1 from a combination of organic and inorganic sources ŽSchroeder et al., 1990; Knud-Hansen et al., 1991b.. Experience suggests that this represents the upper limit to N loading of fish ponds without degradation of water quality. Smaller amounts of N may be added from water supplied to replace losses due to evaporation and seepage, or from atmospheric deposition, particularly during the dry season in the tropics. 2.2. Nitrogen fixation Nitrogen may be added to fish ponds by the reduction of atmospheric dinitrogen by heterocystous cyanobacteria. Nitrogen fixation ranged from 6 to 23 mg N my2 dy1 during the dry season and 21 to 57 mg N my2 dy1 during the rainy season in tropical fish ponds ŽLin et al., 1988.. Nitrogen fixation averaged 24 mg N my2 dy1 in a tropical freshwater fish pond and accounted for 10% of estimated N input ŽAcosta-Nassar et al., 1994.. El Samra and Olah ´ Ž1979. measured an average nitrogen fixation rate of 4 mg N y2 y1 m d in a temperate aquaculture pond. The quantity of N added to aquaculture J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 185 ponds by fixation depends largely upon species composition of the phytoplankton community Žsignificant proportion of heterocystous cyanobacteria. and ammonia concentration. The extent of inhibition of N fixation is inversely related to ammonia concentration ŽLin et al., 1988.. Nitrogen fixation is a minor, but occasionally important contributor to the N budget of aquaculture ponds receiving formulated feeds. 2.3. Phytoplankton uptake of inorganic nitrogen Phytoplankton uptake of DIN from the water column of aquaculture ponds is the primary pathway of nitrogen removal. Semi-intensive aquaculture ponds often develop dense phytoplankton populations Žchlorophyll a ) 250 mg ly1 , Secchi disk visibility - 20 cm. in response to a high rate of nutrient input. Phytoplankton blooms in most fed aquaculture ponds are likely light-limited ŽLaws and Malecha, 1981; Smith and Piedrahita, 1988., suggesting nutrients are available at concentrations exceeding those limiting uptake or are supplied in excess of cellular requirements. Nitrogen uptake by phytoplankton can be estimated by several methods, all yielding results of similar magnitude. Phytoplankton carbon fixation in temperate fish ponds varies from 1 to 3 g C my2 dy1 over an annual cycle ŽBoyd, 1990.. In tropical ponds, carbon fixation by phytoplankton can approach 5 to 10 g C my2 dy1 ŽKrom et al., 1989; Schroeder et al., 1991.. Assuming phytoplankton uptake of nutrients is approximately proportional to the Redfield ratio ŽC:N:Ps 106:16:1., N uptake ranges from about 150 to 450 mg N my2 dy1 in temperate ponds, and from 750 to 1500 mg N my2 dy1 in tropical ponds ŽTable 2.. Sustained Ž1 to 3 month. phytoplankton production of 15 to Table 2 Estimated magnitude of and primary factors affecting the important nitrogen processes in aquaculture ponds Process Rate Žmg my2 dy1 . Primary factors affecting rate Excretion Žgills. Žfecal. Nitrogen fixation 0–300 70–100 0–50 feeding rate, dietary protein feeding rate ammonia concentration, heterocystous cyanobacteria 0–450 750–1500 0–50 ? 25–150 phytoplankton density temperature pH, temperature, wind speed soil mineralogy temperature, overlying water DO 25 150 25–50 temperature ammonia concentration temperature, sediment O 2 penetration variable organic matter C:N Phytoplankton uptake Žtemperate. Žtropical. Ammonia volatilization Ammonium adsorption Sediment–water ammonia flux Nitrification Žsummer. Žspingrfall. Coupled nitrification– denitrification Organic matter accumulation Žburial. 186 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 25 g dry matter my2 dy1 in algal mass cultures has been demonstrated, and higher production Ž30 to 40 g my2 dy1 . was possible over shorter periods ŽGoldman, 1979.. Assuming the N content of phytoplankton with no nutrient deficiency is 5 to 10% of dry matter ŽJørgensen et al., 1991., maximum N assimilation under light-limited conditions typical of eutrophic aquaculture ponds is equivalent to about 750 to 2000 mg N my2 dy1 , although higher uptake rates are possible in algal mass cultures grown under optimum conditions ŽGoldman, 1979.. A third approach toward assessment of the magnitude of phytoplanktonic N uptake can be derived from maximum uptake rates Ž Vmax . determined for natural populations of Microcystis aeruginosa and Oscillatoria agardhii, common cyanobacteria in hypereutrophic aquaculture ponds. Assuming a chlorophyll a concentration of 250 mg ly1 , a chlorophyll a composition of 1.5% of phytoplankton dry weight and Vmax ranging from 1.5 to 4.0 mg N mg dry weighty1 hy1 ŽKappers, 1980., then nitrogen uptake rates range from 600 to 1600 mg N my2 dy1 . Clearly, phytoplankton uptake is a powerful mechanism for conversion of potentially-toxic inorganic N to relatively-stable organic N. Ammonia is the preferred N substrate for phytoplankton, and only after it has been depleted Ž- 0.03 mg N ly1 . will significant quantities of nitrate be assimilated ŽSyrett, 1981; McCarthy, 1981.. Nitrate assimilation and incorporation is an energetically less-favorable pathway of N nutrition for phytoplankton, as enzymatic-reduction to ammonia within the phytoplankton cell is necessary before incorporation into cellular amino acids. Dissolved inorganic nitrogen uptake generally follows Michaelis–Menten enzyme– substrate kinetics in which uptake rate is a hyperbolic function of concentration. Half-saturation concentrations Ž K s . for the assimilation of DIN by marine phytoplankton range from 0.01 to 0.10 mg N ly1 ŽEppley et al., 1969., although internal concentrations required to saturate internal enzyme systems may be 1 to 2 orders of magnitude greater ŽSyrett, 1981. suggesting that nutrients are concentrated within the phytoplankton cell. Given the generally elevated DIN concentrations in semi-intensive aquaculture ponds Ž0.5 to 3 mg ly1 ., it is not likely that substrate concentrations limit phytoplankton growth. In aquaculture ponds, the regulation of DIN concentration is mediated primarily by phytoplankton ŽTucker et al., 1984; Krom et al., 1989.. In these studies, short-term variation in ammonia concentration was inversely related to phytoplankton density. During phytoplankton die-offs, ammonia concentration increased dramatically. As phytoplankton density increased, ammonia concentration declined. In addition, seasonal changes in phytoplankton density affect DIN concentrations in aquaculture ponds ŽTucker and van der Ploeg, 1993.. Dissolved inorganic nitrogen concentrations in commercial catfish ponds were greatest in winter when phytoplankton density was lowest, despite seasonally minimal feeding rates and temperature. Dissolved inorganic nitrogen concentrations may be affected by phytoplankton species composition. In Israeli brackishwater fish ponds, chlorophytes and chrysophytes dominated phytoplankton blooms in winter and spring, whereas cyanobacteria were dominant in summer Žvan Rijn et al., 1986.. The presence of cyanobacteria was coincident with low Ž- 0.01 mg N ly1 . concentrations of DIN. A similar successional J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 187 pattern was observed in commercial catfish ponds ŽTucker and van der Ploeg, 1993., although cyanobacteria were dominant throughout the year. 2.4. Ammonia Õolatilization The equilibrium between gaseous, unionized ammonia ŽNH 3 . and aqueous, ionized . ammonium ŽNHq 4 , which has a p K a of 9.24 at 258C, is strongly affected by pH and much less strongly affected by temperature. Alkaline pH and higher temperature favors the unionized, gaseous form. As a crude approximation, at pH 9.3, about 50% of ammonia is unionized; at pH 8.3, about 10% is unionized; and, at pH 7.3, about 1% is unionized. Volatilization is thus enhanced at elevated pH due to equilibrium relationships and the resultant increase in the partial pressure of ammonia gas. Ammonia volatilization is not important at pH - 7.5. Volatilization may be important as a mechanism of ammonia removal during the late afternoon in poorly-buffered Žtotal alkalinity- 20 mg ly1 as CaCO 3 . ponds, when pH may exceed 9 in response to the depletion of CO 2 from solution by phytoplankton ŽHariyadi et al., 1994.. Murphy and Brownlee Ž1981. calculated ammonia volatilization rates in a hypereutrophic lake dominated by Aphanizomenon flos-aquae during the late afternoon ŽpH ) 9. of a windy day that were an order of magnitude greater than the rate of phytoplankton uptake of ammonia. Schroeder Ž1987. estimated ammonia volatilization of 50 mg N my2 dy1 from manure-loaded polyculture ponds at pH 8 and 0.5 mg N ly1 as ammonia. Volatilization was estimated to account for the loss of 30% of N added to an intensive shrimp pond and 8% of N added to a semi-intensive shrimp pond ŽLorenzen et al., 1997.. However, ammonia volatilization was inconsequential as a mechanism of nitrogen removal in a model of a temperate wastewater stabilization pond ŽFerrara and Avci, 1982.. During summer, when environmental conditions favor volatilization, ammonia concentrations were seasonally minimal. In general, ammonia volatilization is enhanced by increased ammonia concentration, pH, temperature, evaporation rate and wind speed. 2.5. Processes associated with organic matter 2.5.1. Sedimentation and resuspension Aquaculture ponds are generally shallow, characterized in part by minimal organic matter decomposition within truncated water columns. Organic inputs, senescent phytoplankton, fish fecal solids and uneaten feed settle from the water column to the sediment. In ponds fertilized by manures or agricultural by-products, direct consumption by fish is minimal and most of the input settles to the sediment. In addition, as much as 50% of the algal standing crop Žabout 10 g algal dry weight my2 dy1 . may settle to the sediment surface each day ŽSchroeder et al., 1991.. A simulation model that partitioned the fate of N added to semi-intensive shrimp ponds predicted that 48 to 66% would settle to the pond bottom in the form of phytoplankton ŽLorenzen et al., 1997.. Sediment traps in freshwater fish ponds collected 200 to 500 g dry matter my2 dy1 , most derived from previously-deposited material resuspended by the foraging activity of fish ŽSchroeder et al., 1991.. The settling rate of organic matter in intensive shrimp ponds 188 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 can exceed 800 g dry matter my2 dy1 ŽWyban and Sweeney, 1989.. The resuspension of pond sediments has rendered accurate estimation of organic deposition difficult. Greater mineralization of the easily-decomposed fraction of settled organic matter Že.g., phytoplankton. may occur in the water column during resuspension than in the sediment ŽOvernell et al., 1995.. 2.5.2. Regeneration (mineralization) and diffusion Settled particulate organic matter develops into a dynamic, flocculent layer at the sediment–water interface ŽVisscher and Duerr, 1991; Hopkins et al., 1994.. Schroeder Ž1987. demonstrated maximum heterotrophic activity in the flocculent sediment layer extending 2 cm above the firm sediment surface by measuring the rate of weight loss of cotton cloth. In shrimp ponds enriched by bagasse-based pellets, microbial biomass and density increased with the depth of the flocculent layer ŽVisscher and Duerr, 1991.. Microbial density of all functional groups was maximum in the turbid layer above the sediment of an experimental fish tank when compared to densities in the water column and sediment ŽRam et al., 1981.. The extent of decomposition of organic matter in the water column of shallow aquaculture ponds is minimal compared to that occurring at the sediment–water interface. Mineralization of organic matter and the consequent regeneration of nutrients at the sediment–water interface of aquaculture ponds is important as a source of ammonia to the water column and a sink for dissolved oxygen. A simulation model describing ammonia dynamics in commercial catfish ponds estimated that 25 to 33% of the ammonia supplied to the water column was derived from the sediment ŽHargreaves, 1997.. The rate of decomposition of organic matter deposited at the sediment–water interface is likely very rapid. The quality of recently-deposited organic matter is high Žlow C:N ratio. and the half-life of organic N deposited to sediments is likely on the order of 1 to 2 weeks ŽNixon and Pilson, 1983.. In addition, sediment ammonia flux increased rapidly Žwithin days. in response to a pulsed input of plankton-derived particulate organic matter and returned to background rates only after 1 to 2 months ŽKelly and Nixon, 1984; Jensen et al., 1990.. In San Francisco Bay sediments, the rate of sediment ammonia production is directly related to sediment C and N content ŽCaffrey, 1995.. Thus, a substantial fraction of the organic N settling to the sediment is rapidly mineralized and returned to the water column as ammonia. Dissolved organic nitrogen ŽDON. is produced by the autolysis of settled phytoplankton cells or the hydrolysis of other particulate organic N. DON is further mineralized by proteolytic, heterotrophic bacteria to dissolved inorganic substances Že.g., ammonia produced by deamination of DON.. Jana and Roy Ž1985. measured seasonal variation in the abundance of mineralizing bacteria in fish pond sediment over three years. Abundance of protein mineralizing bacteria Ž10 4 to 10 5 cells gy1 . and ammonifying bacteria Ž10 5 to 10 6 cells gy1 . were maximum during winter ŽNovember to January. and minimum during March and September. Bacterial density was directly related to management intensity, although site-specific differences were also apparent. Despite the relatively high efficiency of organic matter decomposition mediated by aerobic heterotrophic bacteria and the deposition and rapid mineralization of high J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 189 quality organic matter at the sediment surface, most decomposition in sediments takes place in the anaerobic layer where the quality of the accumulated organic matter is low Žhigh C:N ratio., and therefore, relatively recalcitrant to decomposition Že.g., fulvic and humic acids.. Foree et al. Ž1971. found that a large quantity of nitrogen in phytoplankton cells was not mineralized after one half to one year of aerobic Ž50%. or anaerobic Ž60%. decomposition. Anaerobic decomposition is characterized by Ž1. incomplete oxidation of organic matter, Ž2. reduced microbial cell yield per unit substrate, and Ž3. reduced assimilatory requirement for N by anaerobic microbes ŽReddy and Patrick, 1984.. Thus, in general, relatively more N is released from organic matter decomposition under anaerobic conditions. Ammonia accumulates in the reduced sediment layer because the biochemical pathway of ammonia transformation requires oxygen. Concentrations of sediment porewater or interstitial ammonia may be an order of magnitude greater than those of the water column. Schroeder Ž1987. measured porewater ammonia concentrations of 10 mg N ly1 at 1 to 4 cm sediment depth one month after filling a fish pond and 100 mg N ly1 in a manure pile in the same pond. Porewater ammonia concentration increased with pond age and water temperature ŽMasuda and Boyd, 1994.. Porewater ammonia concentration of a 40-year old fish pond was over 20 mg N ly1 . Elevated porewater ammonia concentrations are mostly of concern with respect to the growth and survival of cultivated species with benthic feeding or burrowing habits, particularly crustaceans. The profile of porewater ammonia in sediment is typified by a low concentration at the sediment–water interface that increases rapidly with depth. In response to a concentration gradient, ammonia diffuses from the reduced sediment layer to the oxidized surface where it is subject to oxidation to nitrate or further diffusion to overlying water. The depth of maximum porewater ammonia concentration is a function of organic matter concentration and the rate of diffusion to the sediment–water interface. Ammonia flux from the sediment can be enhanced by the burrowing activities of macrofauna Žbioturbation.. Macrofauna can increase the effective surface area of sediment by 125% ŽHylleberg and Henriksen, 1980.. Benthic invertebrates increased the flux of ammonia from marine sediment by 50%, primarily by the irrigation of burrows that may extend from 8 to 12 cm into the sediment ŽHenriksen et al., 1980; Blackburn and Henriksen, 1983.. The concept of bioturbation has been extended to benthivorous fish, although the functional effects of burrow irrigation by benthos and foraging behavior by benthivorous fish are different. Blackburn et al. Ž1988. attributed 30% of the solute flux from the sediment of a marine fish pond to disturbance by fish. In fish Žtilapia and mrigal. exclosure experiments, Riise and Roos Ž1997. measured greater sediment oxygen uptake, ammonia flux, and denitrification associated with oligochaete burrowing activities inside exclosures. Grazing by benthivorous fish on benthic invertebrates limits the loss of N through denitrification and promotes benthic–pelagic coupling and the internal recycling of N through sediment resuspension ŽBreukelaar et al., 1994; Cline et al., 1994; Riise and Roos, 1997.. To summarize, sediments are a source of ammonia to the water column of aquaculture ponds ŽTable 3.. Most of this ammonia is derived from the regeneration of N from the mineralization of relatively high-quality, recently-settled organic matter at the sediment–water interface. A smaller and variable source of ammonia is derived from 190 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 Table 3 Estimates of ammonia flux Žmg N my2 dy1 . from freshwater, estuarine and marine sediments Ammonia flux Refs. Comments Freshwater 0.3–3.1 2.5–3.6 4.2 Acosta-Nassar et al., 1994 Reddy et al., 1990 Schroeder, 1987 new tropical fish pond Lake Okeechobee, FL manured polyculture pond—diffusive fluxqbenthic regeneration eutrophic lake and river ediments freshwater lake sediment 5–15 -10 Žaerobic. 75 Žanaerobic. 11.4 23 19.6–43.2, 31.2 Žmean. 29–44 65 78 25 Žwinter. 150 Žsummer. 11–159 85 Žmean. 36–168 42–140 185 Estuarine 0–252 10–231 -10–207 43 Žannual mean. 70 77 175 119–271, 197 Žmean. 29–882 Marine 8.8–11.7 10.5 Žmean. 11 Žmean. 22 Žmaximum. 50–148 0–144 6–172 182 370 70–672 Fillos and Swanson, 1975 Rysgaard et al., 1994 Avnimelech, 1984 intensive fish pond—mineralization kinetics model ELA Lake 227, Canada freshwater reservoir sediment; Hesslien, 1977 Erickson and Auer, in press anaerobic release rate; 88C Freedman and Canale, 1977 Cerco, 1989 Wickman and Auer, in press Hargreaves, 1997 White Lake, MI 208C Onodaga Lake, NY simulation model, catfish ponds Smith and Fisher, 1986 Lake Calado, Brazil Hohener and Gachter, 1994 ¨ ¨ Jellison et al., 1993 Riise and Roos, 1997 Lake Sempach, Switzerland Mono Lake, CA polyculture fish pond, Thailand Kemp and Boynton, 1984 Klump and Martens, 1981 Reay et al., 1995 Patuxent River estuary Cape Lookout Bight, NC Chesapeake Bay Callender and Hammond, 1982 Vidal and Morguı, ´ 1995 Phoel et al., 1981 Smith and Fisher, 1986 Potomac River estuary Alfacs Bay, Spain York River estuary, VA Choptank River Sumi and Koike, 1990 Japanese estuary Blackburn et al., 1988 marine fish pond Hargrave et al., 1993 Atlantic salmon cage culture site Blackburn and Henriksen, 1983 Caffrey, 1995 Danish marine sediments North San Francisco Bay South San Francisco Bay Limfjorden, Denmark Cape Lookout Bight, NC Flax Pond Blackburn, 1979 Klump and Martens, 1989 Mackin and Swider, 1989 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 191 mineralization of organic matter in the reduced sediment layer. Ammonia diffuses into the water column in response to a concentration gradient extending from the reduced sediment layer to the sediment–water interface, a process that may be enhanced by macrofauna or sediment resuspension. 2.5.3. Organic matter accumulation Most of the nitrogen in aquaculture pond sediments is associated with organic matter, the accumulation rate of which is variable and largely dependent upon input quality. The settling of organic matter and the accumulation of that fraction of organic matter resistant to decomposition in the sediment was the primary mechanism of nitrogen removal in a model of a wastewater stabilization pond ŽFerrara and Avci, 1982.. Small increases in sediment organic matter Ž0.23% yeary1 . and N Ž0.02% yeary1 . were measured in ponds after eight years of channel catfish culture ŽTucker, 1985.. Similarly, Munsiri et al. Ž1996. measured only small differences in soil N concentrations in young Ž2 to 3.5 years. or old Ž8.4 to 11.5 years. shrimp ponds, and most N accumulated in the upper 2.5 cm of sediment. Using nutrient budget estimates of Schroeder Ž1987. and assuming accumulation in the 0 to 5 cm layer only, N accumulated in sediment by about 0.07% after a 4-month culture period. Organic N of a tropical fish pond sediment increased by about 0.06% after four months, accounting for 65% of input N ŽAcostaNassar et al., 1994.. Small increases in total N of shrimp pond sediment were measured after six months, although spatial variability was more pronounced than temporal variability ŽSmith, 1996.. Organic carbon in the upper 5-cm sediment layer of tropical fish ponds enriched by chicken manure increased by about 0.1% monthy1 ŽAyub et al., 1993.. Similarly, 70% of input N accumulated in the sediments of tropical fish ponds enriched by chicken manure ŽGreen and Boyd, 1995.. Chiba Ž1986. recovered 8 to 13% of input N as sediment organic N in an intensive eel pond with continuous water circulation. Hopkins et al. Ž1994. recovered 15 to 22% of N input to semi-intensive shrimp ponds as bottom organic deposits Žsludge. in which sediment was periodically suspended by aeration or allowed to settle in place. Approximately 31% of input N was calculated to accumulate in a tropical shrimp sediment after 2 to 3 production cycles ŽBriggs and Funge-Smith, 1994.. Despite the addition of large quantities of organic matter to aquaculture ponds, average N concentration of soils from 358 freshwater and 346 brackishwater fish ponds were 0.28% and 0.30%, respectively ŽBoyd et al., 1994a.. 2.6. Ammonium adsorption . Ammonium ŽNHq 4 may weakly adsorb to negatively-charged cation exchange sites on the surface of clay minerals or organic matter in the sediment. Adsorbed Žexchangeable. ammonium is important as a source of ammonia to the overlying water and as a sink for ammonia produced from DON mineralization. Acosta-Nassar et al. Ž1994. estimated that about 2% of the N added to a freshwater fish pond was stored in the adsorbed pool, although undoubtedly greater amounts of adsorbed ammonium were derived from the mineralization of soil autochthonous or previously-deposited sediment organic matter. J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 192 Adsorbed NHq 4 and porewater ammonia are in equilibrium, so profiles of adsorbed NHq and porewater ammonia are similar. The ratio of adsorbed NHq 4 4 to porewater ammonia Žpartition coefficient. is variable, but generally much greater than 1. Differences in the partition coefficient are related to the cation exchange capacity of soil, adsorbed and porewater ammonia concentrations, season Žtemperature. and sediment depth. The concentration of adsorbed ammonium is affected by sediment drying and re-wetting. The exchangeable ammonium pool declined rapidly to very low levels after 6 weeks of drying a fish pond sediment ŽDiab and Shilo, 1986.. Following refilling, the adsorbed ammonium pool increased within 10 days to levels equivalent to about 50% of that before draining and continued to increase during the cropping cycle ŽShilo and Rimon, 1982; Diab and Shilo, 1986.. Presumably, nitrification was responsible for reduction in exchangeable ammonium concentration, although evidence that adsorbed ammonium can be utilized by nitrifying bacteria is equivocal. The loose adsorption of exchangeable ammonium to sediment and the association of nitrifying bacteria with particles are evidence in support of the importance of this process ŽSeitzinger, 1990.. The dynamic nature of the adsorbed ammonium pool is further illustrated by measurement of the complete and rapid desorption of ammonium from a sandy sediment after two hours following suspension by wind-driven water turbulence ŽSimon, 1989.. Similarly, Reddy et al. Ž1996. measured a release rate of ammonia of 67 to 85 mg N my2 miny1 from resuspended sediment collected from Lake Apopka, Florida with most of the release occurring within 15 min. Ammonium supplied to the water column by desorption from sediment solids was estimated to exceed that supplied by diffusive flux. Suspension of aquaculture pond sediments by aeration or wind-driven water turbulence may increase, at least temporarily, the concentration of ammonia in the water column. 2.7. Nitrification Nitrification is the sequential, two-step oxidation of ammonia to nitrate. The process is mediated by predominately two bacterial genera. The oxidation of ammonia is mediated by Nitrosomonas and the oxidation of nitrite is mediated by Nitrobacter. The organisms are chemoautotrophic, gram-negative, motile rods with long generation times Ž20 to 40 h.. The reactions proceed as follows: y q NHq 4 q 1 1r2 O 2 ™ NO 2 q 2H q H 2 O and y NOy 2 q1r2 O 2 ™ NO 3 Thus, two moles of oxygen are required for each mole of NHq 4 oxidized. y These organisms derive energy from the oxidation of NHq 4 and NO 2 . The free q y1 Ž . energy yield DG from the oxidation of NH 4 is about y65 kcal mole , and that from y1 Ž the oxidation of NOy Focht and Verstraete, 1977.. Thus, 2 is about y18 kcal mole y over three times as much NO 2 must be oxidized to support an equivalent microbial growth to that derived from the oxidation of NHq 4. J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 193 Nitrification rates of estuarine sediments range from 15 to 25 mg N my2 dy1 ŽHenriksen and Kemp, 1988. and are probably representative of those of aquaculture pond sediments, although no direct measurements have been made ŽTable 4.. Assuming 5 to 10% of sediment oxygen demand is utilized for nitrification ŽHenriksen and Kemp, 1988. then about 25 to 50 mg N my2 dy1 is oxidized, equivalent to 5 to 10% of daily N input. Thus, the magnitude of nitrification is a relatively small in relation to the rate of other N transformations during the production cycle. Nitrification rates are elevated only during periods between cropping cycles when pond soils are aerated as they dry. Nitrification is affected by dissolved oxygen concentration, temperature, substrate concentration, pH, numbers of nitrifying bacteria, and availability of surfaces. Many of these factors are interrelated and their effect on nitrification is complex. Nitrifying bacteria require oxygen to derive energy from reduced N. The half-saturation concentration Ž K m . for oxygen ranges from 0.3 to 0.9 mg ly1 and is directly related to temperature ŽPainter, 1970.. The K m for oxygen is higher for Nitrobacter than for Nitrosomonas at 308C suggesting that nitrite oxidation is more sensitive to low oxygen Table 4 Nitrification rate Žmg N my2 dy1 . estimates in the sediments of marine and freshwater systems Nitrification rate Refs. LocationrComments 0 0.4–0.9 Žmeans 0.5. 1–35 0–42 4–18 3–48 11 11 13 15 Blackburn et al., 1988 Acosta-Nassar et al., 1994 Riise and Roos, 1997 Henriksen, 1980 Henriksen et al., 1981 Billen, 1978 Blackburn and Henriksen, 1983 Lindau et al., 1988b DeLaune and Lindau, 1989 tropical marine fish pond tropical freshwater fish pond polyculture fish pond, Thailand Danish coast Danish coast Belgian coast ŽNorth Sea. Danish coast rice soil Lac des Allemands, LA Little Lake, LA Danish coast without fauna with fauna Danish coast Scottish estuary Japanese coast Patuxent River estuary Patuxent River estuary Lake Verret, LA Narragansett Bay Japanese coast freshwater lake sediment freshwater stream sediment without fauna with fauna Belgian coast ŽNorth Sea. freshwater lake sediment Calcasieu River, LA Henriksen et al., 1980 16 28–35 7–37 Žmeans 20. 7–45 Žmeans 20. 8–34 Žmeans 22. 24 26–30 30 7–45 Žmeans 39. 27–67 Žmeans 45. 59–76 29 69 63 67 60–152 Hansen et al., 1981 MacFarlane and Herbert, 1984 Nishio et al., 1983 Boynton et al., 1980 Jenkins and Kemp, 1984 DeLaune and Smith, 1987 Seitzinger et al., 1984 Koike and Hattori, 1978 Jensen et al., 1994 Chaterpaul et al., 1980 Vanderborght et al., 1977 Rysgaard et al., 1994 DeLaune et al., 1991 194 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 concentrations at warm temperature. With all other conditions sufficient, nitrification rate is constant at dissolved oxygen concentrations above 2 mg ly1 . The K m for oxygen of nitrifying bacteria is several orders of magnitude greater than that of heterotrophic aerobic bacteria, suggesting that heterotrophic bacteria may be competitively more successful than nitrifying bacteria at low oxygen concentration. Oxygen penetration into sediment is a key factor regulating nitrification ŽReddy and Patrick, 1984; Rysgaard et al., 1994.. The depth of oxygen penetration into aquatic sediments is typically on the order of 1 to 5 mm and is inversely related to temperature ŽRevsbech et al., 1980.. Although nitrification increases with temperature, the volume of sediment involved in nitrification is restricted by the depth of oxygen penetration, which exerts control on overall nitrification rate. Nitrification potential was demonstrated in reduced sediment Ž6 to 8 cm depth. indicating the ability of nitrifying bacteria to survive in anaerobic environments, although actual nitrification was restricted to the sediment surface ŽHansen et al., 1981; Henriksen et al., 1981.. Nitrification activity of dormant, nitrifying bacteria in anoxic sediment layers will increase rapidly Žwithin hours. in response to exposure to oxygen in overlying water ŽJensen et al., 1993.. Nitrification potential was minimum during the summer, coincident with minimum sediment oxygen penetration. The depth of oxygen penetration, and consequently nitrification rate, is also inversely related to the sedimentation of organic matter, which is maximum in warmer months. The optimum temperature range for growth of pure cultures of nitrifying bacteria Ž25 to 358C. is fairly narrow, although the scope for growth Ž3 to 458C. is much wider ŽFocht and Verstraete, 1977.. The Q10 of nitrification ranges from 1.7 to 3.3 between 20 and 308C ŽFenchel and Blackburn, 1979.. Evidence of differential sensitivity of the two principal nitrifying genera to temperature is equivocal, but tends to implicate the greater sensitivity of nitrite oxidizers to low temperature, particularly at pH values outside the optimum range ŽFocht and Verstraete, 1977.. However, climatic and other environmental variables exert strong selection pressures on populations of nitrifying bacteria, suggesting that adaptation to local conditions is also likely. Thus, information derived from laboratory studies of pure cultures should be viewed with qualification. Nitrification rate is also affected by substrate concentration. In aquaculture pond sediments, ammonia is supplied Ž1. by the mineralization of organic N at the sediment– water interface, Ž2. diffusion of ammonia from the reduced sediment layer to the sediment–water interface, and Ž3. the bulk water. Half-saturation concentrations Ž K m . for substrate increase with temperature Ž20 to 328C. and range from 1 to 10 mg N ly1 for ammonia oxidation, and from 5 to 9 mg N ly1 for nitrite oxidation ŽPainter, 1970.. Ammonia concentrations in commercial catfish ponds are usually - 3 mg N ly1 ŽTucker and van der Ploeg, 1993., and the highest concentrations occur during the winter when phytoplankton biomass is minimal. Nitrite concentrations in channel catfish ponds are usually - 0.2 mg N ly1 with seasonal maxima in the spring and fall. Such low concentrations in the bulk water impose substrate limitation on nitrification in aquaculture ponds, suggesting that the kinetics of nitrification are first-order with respect to substrate concentration. However, nutrient regeneration at the sediment–water interface and ammonia diffusion from reduced sediment may be sufficient to surmount substrate limitation. J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 195 Nitrifying bacteria require slightly alkaline pH Ž7 to 8.5. for optimal growth. At pH ) 8.5, Nitrobacter may be inhibited more than Nitrosomonas, resulting in an accumulation of nitrite ŽFenchel and Blackburn, 1979.. Increased nitrification at alkaline pH suggests that NH 3 may be the substrate for nitrification. Also, unionized ammonia can inhibit nitrite oxidation at 0.1 to 1.0 mg NH 3 –N ly1 ŽBelser, 1979.. However, these concentrations are rarely observed in fish ponds as they are also toxic to fish. Finally, pH is important because two hydrogen ions are released for each mole of ammonia oxidized. Natural waters usually contain sufficient alkalinity to buffer an increase in hydrogen ion concentration from nitrification. Nitrifiers are lithotrophic, requiring organic or mineral surfaces for attachment. Nitrifier density in the soil at the sediment surface Ž10 6 to 10 9 cmy3 . is about three orders of magnitude greater than that in the water column Ž10 3 to 10 4 mly1 .. The abundance of ammonia oxidizers Ž10 4 to10 5 cells gy1 . in sediment is greater than that of nitrite oxidizers Ž10 3 cells gy1 . ŽRam et al., 1981; Ram et al., 1982.. The sediment surface is the locus for mineralization of particulate organic matter settling from the water column. In addition, ammonium may be concentrated on sediment mineral particles Žclays. as part of the cation exchange complex. Competition for surfaces between heterotrophic and nitrifying bacteria may contribute to limitation of population density of the latter group. Nitrification at the sediment–water interface is more important than nitrification in the water column in stratified or periodically-mixed fish ponds. Nitrification in the water column is restricted by the availability of surfaces and possibly by light inhibition. Nitrification may increase temporarily following phytoplankton die-offs in response to elevated ammonia concentration. Water column nitrification is an important mechanism of ammonia transformation in high-intensity pond systems in which particles suspended by mechanical aeration are sites of active mineralization and nitrification. In flooded soils, nitrification and denitrification are closely coupled. A two-layer model has been developed to describe the interdependence of these two processes ŽReddy and Patrick, 1984.. By the two-layer model, ammonia diffuses from the reduced sediment layer along a concentration gradient to the surface, where it is oxidized by nitrifying bacteria. Nitrate diffuses in response to a concentration gradient to the reduced sediment layer where it is denitrified to dinitrogen gas that evolves to the atmosphere through gas ebullition. Thus, although oxygen inhibits denitrification, the reaction indirectly requires oxygen for the production of nitrate. A complementary theory has been developed to explain the seemingly contradictory coexistence of oxic and anoxic processes within an oxic environment. Jørgensen Ž1977. found that detrital particles of 100 mm to several mm may have anoxic centers. Paerl Ž1984. estimated that detrital aggregates, biofilms, microbial mats and planktonic symbioses ranging from 100 mm to several mm in thickness can have reduced microzones ŽPaerl, 1984; Paerl and Pinckney, 1996.. Jenkins and Kemp Ž1984. argued that calculation of the effective nitrate diffusion distance Žf 80 mm. suggests that denitrification must be tightly coupled with nitrification and occur in reduced microzones within the oxidized layer of the sediment surface. The quantity of reduced microsites depends on Ž1. oxygen consumption rate, Ž2. oxygen diffusion rate, and Ž3. particle geometry ŽFocht and Verstraete, 1977.. 196 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 The pattern of nitrification following the establishment of conditions favorable for process development is characterized by the rapid oxidation of ammonia, an accumulation of nitrite coincident with a decline in ammonia, and after a lag period, a decline in NOy 2 . This characteristic pattern explains, in part, the bimodal distribution of annual nitrite concentration maxima measured in warm temperate commercial catfish ponds ŽTucker and van der Ploeg, 1993.. Interpretation of factor analysis of the data of Tucker and van der Ploeg Ž1993. suggested that sediment oxygenation was an important regulator of nitrification in these ponds ŽHargreaves and Tucker, 1996.. During the summer, nitrification in aquaculture pond sediments is most likely limited by the depth of oxygen penetration Žtypically 1 to 5 mm.. In estuarine sediments, the summer depression of nitrification rate has been attributed to limited oxygen diffusion into sediments ŽHansen et al., 1981; Jenkins and Kemp, 1984.. During the summer, the rate of input of organic matter to aquaculture pond sediment is maximum due to maximum feeding rates and standing crops of phytoplankton, and are coincident with maximum seasonal temperatures. The decomposition of recently deposited organic matter by large and active populations of aerobic, heterotrophic bacteria limit the diffusion of oxygen into sediment. Although operation of aerators may prevent nearsediment dissolved oxygen from declining to concentrations - 2 mg ly1 , it is likely that a laminar benthic boundary layer Žf 100 mm. depleted of dissolved oxygen develops at the sediment–water interface in the summer. Stirring of sediments during pond aeration may increase the depth of oxygen diffusion ŽRevsbech et al., 1980.. In the water column, nitrification is low because ammonia is present at substrate-limiting concentrations due to rapid uptake by large and actively-growing phytoplankton populations. As temperature declines during the fall, dissolved oxygen concentration of the water column increases due to reduced feeding rate and pond respiration and increased oxygen solubility. Sediment oxygen demand declines as metabolic activity of bacteria is depressed by cooler temperatures and reduced inputs of organic matter from the water column. Consequently, the depth of oxygen penetration into the sediment surface increases, thereby increasing the volume of sediment that is involved in nitrification. In the water column, nitrification is stimulated by increases in ammonia resulting from reduced uptake by phytoplankton. Nitrification rate is reduced during the winter due to seasonally minimal temperatures. In the spring, as temperature increases, organic N accumulated is rapidly mineralized to ammonia and the rate of nitrification is once again stimulated, producing another sharp increase in water column nitrite concentration. As temperature increases further, water column dissolved oxygen declines, sediment oxygen penetration and nitrification are reduced. In summary, the interaction between temperature and the depth of sediment oxygen penetration exerts control over nitrification in fish pond sediments. The interaction between temperature and substrate concentration exerts control over nitrification in the water column. During summer in catfish ponds sediment nitrification is controlled Žlimited. by oxygen penetration into the sediment and low substrate concentrations in the water column, despite seasonally maximum temperatures. During the fall, control of nitrification shifts from oxygen penetration Žsediment. or substrate concentration Žwater column. to temperature. During the winter, low temperature limits nitrification. During J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 197 the spring, control of nitrification shifts from temperature to sediment oxygen penetration. 2.8. Nitrate reduction Nitrate may follow several biochemical pathways following production by nitrification. Plants and microbes may reduce nitrate to ammonia for incorporation into cellular amino acids Žassimilatory nitrate reduction.. Nitrate may function as a terminal electron acceptor during the oxidation of organic matter and thereby supply energy for microbial growth. Nitrate respiration results in the reduction of nitrate to dinitrogen Ždenitrification. or ammonia Ždissimilatory nitrate reduction to ammonia.. y NOy 3 ™ NO 2 ™ NO ™ N2 O ™ N2 Oxygen is the energetically preferred terminal electron acceptor for the oxidation of organic matter. However, when oxygen concentration becomes limiting Ž; 0.1 to 0.2 mg ly1 or E h - 220 mV., heterotrophic facultative anaerobes shift to nitrate as the terminal electron acceptor. The energetic yield from the oxidation of organic carbon Že.g., glucose. by nitrate Ž DG s y649 kcal moley1 . is only slightly less than that by oxygen Ž DG s y686 kcal moley1 .. Unlike the limited species diversity of bacteria mediating nitrification, at least 14 genera of bacteria can reduce nitrate, and Pseudomonas, Bacillus and Alcaligines are the most prominent numerically ŽFocht and Verstraete, 1977.. Also, the growth, activity and population density of denitrifying bacteria exceed that of nitrifying bacteria. Most denitrifying bacteria are considered facultative anaerobes. Although denitrification is inhibited by oxygen, the reaction occurs primarily near the sediment surface, possibly in reduced Žsuboxic. microzones in the oxidized sediment surface layer. The rate of denitrification depends on temperature, concentrations of nitrate, organic carbon, and oxygen, and the population density of denitrifying bacteria ŽTable 5.. Denitrification rates increase with substrate concentration. Denitrification rates in estuaries correspond with seasonal Žspring. peaks in nitrate loading ŽAndersen et al., 1984.. However, denitrification rates in most natural aquatic systems are first order with respect to nitrate concentration, and can be considered substrate limited. In aquaculture ponds, nitrate is typically - 0.5 mg N ly1 ŽZiemann et al., 1992; Tucker and van der Ploeg, 1993., a concentration likely below reported half-saturation constants Ž K m . for denitrification. Nitrate concentrations in temperate aquaculture ponds are maximum during winter, when phytoplankton blooms are minimal. Kinetic constants vary with available carbon Žreductant.. Reported K m values range from 0.1 to 170 mg N ly1 , and increase in direct relation to carbon ŽFocht and Verstraete, 1977.. In a multiple Žstepwise. regression model, dissolved organic carbon concentration was the most important predictor of denitrifying bacteria abundance in tropical fish ponds ŽJana and Patel, 1985.. The large quantity and low C:N ratio of settled organic matter in aquaculture ponds suggests that carbon limitation of denitrification is not likely. Aquatic sediments consist of a very thin oxidized layer overlying a much thicker anoxic layer. Therefore, the potential for denitrification in fish ponds is very high. J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 198 Table 5 Denitrification rate Žmg N my2 dy1 . estimates in the sediments of marine and freshwater systems Denitrification rate Refs. LocationrComments 1.4–3.6 Messer and Brezonik, 1983 3.6–7.1 0.1–7.4 2.3 Acosta-Nassar et al., 1994 Oren and Blackburn, 1979 2.7–10.9 3.6–7.2 5 3.4–13 3.6–18 3.8 Kaspar, 1982 Chan and Knowles, 1979 Tiren, ´ 1977 Nishio et al., 1983 Sweerts and de Beer, 1989 Smith and DeLaune, 1983 0–29 4–55 Billen, 1978 Cerco, 1989 4–71 10–40 14 14–20 18–35 17–34 - 25 25–40 26–30 29 1.5–57 47–81 Andersen et al., 1984 Henriksen et al., 1980 Sørensen, 1978 Chan and Campbell, 1980 Nielsen, 1992 Seitzinger et al., 1984 Rysgaard et al., 1994 Tiren, ´ 1977 Jenkins and Kemp, 1984 Vanderborght et al., 1977 Lindau et al., 1990 Roos and Eriksen, 1995 Blackburn et al., 1988 Lake Okeechobee acetylene blockage mass balance tropical freshwater fish pond Kysing Fjord, Denmark Ž ; 0.15 mg ly1 NOy . 3 –N intertidal mud flat eutrophic ponds oligotrophic Swedish lake Japanese coast eutrophic lake ŽVechten. freshwaterrestuarine eutrophic lake sediments Belgian coast Potomac River Ž10–308C, 8 mg ly1 DO, . 0.21–0.63 mg ly1 NOy 3 –N Danish estuary; seasonal variation Danish coast Danish coast eutrophic Canadian lake eutrophic stream bed Narragansett Bay freshwater sediment 3 eutrophic Swedish lakes Patuxent River estuary Žspring. Belgian coast urea-treated rice plot semi-intensive polyculture pond marine fish ponds acetylene blockage nitriteqnitrate reduction marine fish ponds 14–25 71–119 56–69 Krom, unpublished Žcited in Blackburn et al., 1988. D’Angelo and D’Angelo, 1993 Riise and Roos, 1997 Andersen, 1977 52 57 58 110 34 85 100–500 45 34–52 95–160 100–200 101–296 367 DeLaune and Smith, 1987 DeLaune et al., 1991 van Kessel, 1977 Nishio et al., 1982 Seitzinger and Nixon, 1985 Lindau et al., 1988a 33–342 420–490 Lindau et al., 1990 Binnerup et al., 1992 Lake Okeechobee polyculture fish ponds, Thailand Byrup Langsø Žlab cores. Byrup Langsø Žmass balance. Kvind Sø Žlab cores. Kvind Sø Žmass balance. enriched lake sediment Lake Verret, LA—nitrate reduction Calcasieu River, LA enriched ditch sediment polluted estuary, Japan enriched marine mesocosm enriched bottomland hard-wood forest swamp plot KNO 3 -treated rice plots enriched, bioturbated marine sediment J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 199 Although denitrification is an anaerobic process, it is largely dependent on oxygen concentration for the production of nitrate through nitrification. Factors that stimulate nitrification Že.g., warm temperature, abundant oxygen. will also stimulate denitrification. In aquatic sediments in which the nitrate concentration in the overlying water is low, the denitrification rate will be limited by the nitrification rate, which in turn is regulated by the depth of sediment oxygen penetration ŽRysgaard et al., 1994; Jensen et al., 1994.. The presence of an oxidized sediment layer also increases the diffusion distance of nitrate from the overlying water to anoxic sediment thereby reducing the rate of denitrification of nitrate derived from the overlying water. A wide range of Q10 values have been reported, possibly reflecting the broad generic diversity of denitrifying bacteria. Most Q10 values range from 1.4 to 3.4 between 15 and 358C ŽFocht and Verstraete, 1977.. Denitrifier activity is sharply curtailed below 158C. Q10 values are affected by the concentration of oxidant Žnitrate. and reductant Žorganic carbon. as well as oxygen concentration. At 348C denitrification rate was much less affected by oxygen concentration than at 198C ŽFocht and Verstraete, 1977.. The abundance of denitryifying bacteria in tropical fish pond sediment was maximum during summer Ž10 4 cells gy1 . and minimum during winter Ž10 3 cells gy1 . ŽJana and Patel, 1985.. Comparable abundance and seasonal patterns were observed in the water column. In Israeli fish pond sediment, the abundance of denitrifying bacteria increased with intensity of management and ranged from 10 4 to 10 6 cells gy1 ŽRam et al., 1982.. 3. Management practices affecting nitrogen biogeochemistry 3.1. Feeds and feeding practices Feeds and feeding practices have a dramatic impact on ammonia concentration in fish pond water. Ammonia was strongly correlated with daily feeding rate in channel catfish ponds over the range 0 to 224 kg hay1 dy1 ŽTucker et al., 1979; Cole and Boyd, 1986.. Ammonia increased in response to dietary protein concentration and total protein fed over the range 24% to 40% ŽLi and Lovell, 1992.. However, un-ionized ammonia ŽNH 3 . concentration was not affected by dietary protein concentration. Temporary withdrawal of feed Ž9 days. did not reduce ammonia in channel catfish ponds ŽTidwell et al., 1994.. Ammonia concentration was not different in channel catfish ponds in which fish were fed once daily to satiation at 0830 h, 1600 h, 2000 h, or with demand feeders ŽRobinson et al., 1995.. 3.2. Water exchange Various water management practices have been evaluated to reduce ammonia concentration in fish ponds. Water exchange rates of 0, 1, 2 or 4 pond volumes over three months ŽJuly to September. were insufficient to affect water quality in channel catfish ponds ŽMcGee and Boyd, 1983.. A simulation model of semi-intensive shrimp ponds predicted that ammonia concentrations would be minimum with no water exchange, 200 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 increase to a maximum at water exchange rates of 0.2 to 0.4 dy1 , and decrease at water exchange rates exceeding 0.4 dy1 ŽLorenzen et al., 1997.. A water exchange rate of 0.025 dy1 was sufficient to reduce Ž P - 0.05. ammonia concentration in intensive Ž44 my2 . shrimp ponds compared to ponds with no water exchange ŽHopkins et al., 1993.. Ammonia concentration in ponds with a water exchange rate of 0.25 dy1 was not different from that of inlet water. In high-biomass Ž) 10 kg my2 ., intensive fish ponds Ž500 m3 ., a hydraulic retention time ) 24 h in rearing units was necessary for nitrification to proceed to completion ŽDiab et al., 1992.. Greater water exchange rates led to washout of nitrifying bacteria. 3.3. Water circulation and aeration Semi-intensive pond systems for the culture of channel catfish and penaeid shrimp employ paddlewheel aeration to maintain dissolved oxygen concentration. The effects of aeration and circulation on DIN concentrations are a complex function of feeding rate, sediment suspension, duration of aeration and phytoplankton density. Ammonia concentration was only slightly lower Ž P ) 0.05. and nitrite concentration slightly higher Ž P ) 0.05. in channel catfish ponds Ž50 kg feed hay1 dy1 . aerated for 6 h during the night as compared to ponds aerated on an emergency basis only ŽLai-Fa and Boyd, 1988.. Ammonia concentration increased slightly and nitrite concentration increased substantially in channel catfish ponds Žup to 90 kg feed hay1 dy1 . aerated nightly compared to those of unaerated control ponds ŽHollerman and Boyd, 1980.. Similarly, concentrations of ammonia, nitrite and nitrate were directly related to duration of aeration Žemergency, nightly, continuous. in channel catfish ponds ŽThomforde and Boyd, 1991.. The suspension of sediment particles by aeration may have promoted rapid desorption of exchangeable ammonium and stimulated nitrification in the water column. Continuous paddlewheel aeration reduced ammonia concentrations slightly in brackishwater shrimp ponds, but concentrations were not different from unaerated ponds ŽSanares et al., 1986.. Un-ionized ammonia concentrations were not affected by continuous paddlewheel aeration in freshwater ponds stocked with tilapia at 3000 kg hay1 ŽVer and Chiu, 1986.. In Taiwan, Israel and Hawaii, intensive pond systems have been developed in which water is circulated continuously by paddlewheel aeration, and water and settled organic matter are periodically or continuously removed from a center drain ŽAvnimelech et al., 1986; Wyban and Sweeney, 1989; Fast and Boyd, 1992.. Phytoplankton uptake is insufficient to assimilate the large quantity of ammonia generated as a consequence of high feeding rate and stocking density. In such high-intensity ponds, nitrification in the water column is the most important mechanism of ammonia transformation. Despite nitrate accumulation in the water of such circulated systems, the sediment was assumed to be the site of substantial denitrification. Total N may exceed 30 mg N ly1 Žmostly present as nitrate. ŽAvnimelech et al., 1986.. Treatment of effluent discharged from intensive circulated water systems must address solid Žphytoplankton. and dissolved Žnutrient. components ŽLorenzen et al., 1997.. High-intensity pond systems have been integrated with larger, extensive reservoirs. Hydraulic detention time in the intensive component is sufficient to allow water-column J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 201 nitrification to proceed to completion. Effluent is directed to the reservoir, where solids are deposited and denitrification takes place before recirculation to the high-intensity ponds. 3.4. Pond depth In shrimp ponds, ammonia concentration was not significantly affected by pond depth, although nitrite and nitrate were inversely related to pond depth ŽCarpenter et al., 1986.. Presumably, reducing water depth in a pond with a high phytoplankton density will reduce light limitation of phytoplankton growth and thereby enhance nutrient uptake ŽPiedrahita, 1991.. 3.5. Organic carbon addition Avnimelech et al. Ž1989. demonstrated a practical technique to recycle excess N into fish. Dissolved inorganic nitrogen limitation can be established in intensive, circulated fish ponds by adding a carbon-rich substrate Že.g., cellulose, sorghum meal. that promotes the formation of microbial biomass. The resulting heterotrophic production Žsingle-cell protein. may be utilized as a food source by carp and tilapia ŽSchroeder, 1978; Beveridge et al., 1989; Rahmatullah and Beveridge, 1993.. 3.6. Microbial augmentation Microbial augmentation refers to the supplementation of pond waters or soils with concentrated bacterial suspensions with the goal of reducing soil organic matter, improving dissolved oxygen concentration and removal of ammonia. In studies conducted in shrimp and channel catfish ponds, differences in shrimp or fish production and ammonia, nitrite and nitrate concentrations in ponds supplemented with bacteria was not significantly different from that of untreated control ponds ŽBoyd et al., 1984; Tucker and Lloyd, 1985b; Chiayvareesajja and Boyd, 1993; Queiroz and Boyd, 1998.. 3.7. Ion exchange Ion exchange is a well-known and effective means of removing ammonium from water in recirculating fish culture systems ŽSpotte, 1979.. Naturally-occurring ion exchange materials, such as the zeolite clinoptilolite, have been added to shrimp ponds at 200 kg hay1 monthy1 ŽChien, 1992. to 380 kg hay1 monthy1 ŽBriggs and Funge-Smith, 1996.. The efficacy of ion exchange is affected by the ionic strength of water, by occlusion of exchange sites by dissolved organic carbon, and by the particle size of the exchange resin ŽSpotte, 1979.. In general, the removal of ammonium from water is reduced as salinity increases. Briggs and Funge-Smith Ž1996. demonstrated no removal of ammonium at salinities ranging from 0 to 30 ppt and concluded that the application of ion exchange materials to shrimp ponds was not effective. 202 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 3.8. Sediment management Most sediment management techniques are undertaken while the pond is drained between cropping cycles. Drying is probably the most important, practical, and cost-effective sediment management technique. Drying promotes oxidation of accumulated organic matter ŽAyub et al., 1993. and nitrification of mineralized N ŽDiab and Shilo, 1986., although the optimum soil moisture content for organic matter decomposition is about 20% ŽBoyd, 1992.. Shrimp pond soils in Ecuador are dried for an average of 10 days after harvest ŽPeterson and Daniels, 1992.. Pond soils may be tilled to hasten the decomposition process, although five weeks of drying are required before heavy equipment can enter the pond. Organic matter may be physically removed from intensive shrimp ponds manually, by suction dredges or earthmoving equipment, or flushed out by hydraulic jets ŽClifford, 1992., although these practices have potentially negative environmental impacts associated with the discharge of organically-enriched effluent, and further, the efficacy of these practices is questionable. The effect of two sediment management practices on soil chemical properties from two shrimp farms was evaluated in Australia ŽSmith, 1996.. One one farm sediments were removed following the cropping cycle and on the other sediments were redistributed following drying. No difference in total N was detected in soils from the two farms. Given the similar chemical composition of new shrimp pond soils to piles of excavated sediment, particularly with respect to organic matter concentration, the practice of sediment removal from shrimp ponds appears unjustified ŽBoyd et al., 1994b.. Ponds may be limed after draining and drying to raise soil pH to levels promoting decomposition, particularly in brackishwater ponds constructed on acid-sulfate soil and in areas with low alkalinity water supplies. Ponds are typically limed at 1000 to 3000 kg hay1 depending on soil pH ŽBoyd, 1992.. Fertilization of brackishwater shrimp pond soils by 50 to 200 kg urea hay1 reduced sediment organic matter ŽPeterson and Daniels, 1992. although urea application did not reduce organic carbon in manured freshwater fish ponds ŽAyub et al., 1993.. Sediment management techniques during the cropping cycle while the pond is full have not been fully evaluated. Brackishwater shrimp ponds may be dredged during the cropping cycle to remove accumulated organic matter or a chain may be dragged across the pond bottom periodically ŽCosta-Pierce and Pullin, 1989; Fast and Boyd, 1992; Beveridge et al., 1994.. 3.9. Sediment management implications Management approaches toward sediments can be divided into two types based upon the desired goal. In ponds receiving nutrients supplied in excess of assimilatory capacity, or where autotrophic food webs are not important for increased fish yields, but are only important for water quality management, the promotion of conditions that maximize the potential of the pond to remove excess N is desirable. Dentrification is the process with the greatest potential to remove N although the preliminary transformation of reduced Žammonia. to oxidized Žnitrate. N is required. Management techniques that improve oxic J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 203 conditions at the sediment–water interface will promote rapid mineralization and coupled nitrification–denitrification. Likewise, techniques that promote water-column nitrification will increase substrate in the bulk water to concentrations that will stimulate sediment denitrification. For ponds in which fish yields are based on primary productivity, promotion of nutrient recycling within the pond will maximize nutrient availability for phytoplankton. Anaerobic sediment conditions will allow the diffusion of ammonia mineralized under reduced conditions or regenerated at the sediment–water interface to diffuse into the water column where it will be available for phytoplankton. However, this goal is incompatible with the management requirement of maintaining adequate dissolved oxygen for fish production. 4. Research needs Much of the research on nitrogen cycling in shallow aquatic ecosystems has been conducted in estuarine or lacustrine environments. Much of this information is directly applicable and relevant to describing rates and controlling factors of various N transformation processes in aquaculture ponds. However few controlled studies of N cycling, specifically directed toward the unique circumstances prevalent in earthen aquaculture ponds, have been carried out and there are several important gaps in information that remain to be filled. The design and conduct of experiments should be formulated with a view toward the development of practical management procedures that enhance fish growth and production. Of primary concern is a more complete understanding of factors regulating the concentrations of the two nitrogenous compounds with potential toxicity to cultured organisms—ammonia and nitrite. Concentration reductions can be achieved by a decrease in the production rate or an increase in the removal rates of each of these compounds. Although phytoplankton management is an elusive goal of aquaculturists and currently beyond the scope of management control in pond culture, research efforts directed toward regulation of phytoplankton biomass, activity and community composition has profound implications for the maintenance of water quality conditions favorable for fish production. Generally, conditions that promote rapid rates of primary production tend to result in low ammonia concentration. In addition, the interacting roles of the factors that regulate nitrification Žtemperature, oxygen and substrate concentration. in the water and the sediment of aquaculture ponds require elucidation. Of secondary interest, processes related to the interaction between the sediment and the water column of aquaculture ponds are poorly understood. The role of the sediment as a source of ammonia to the overlying water and practical management techniques to limit the rate of sediment diffusion are necessary. At this time, the effect of depositional events, such as the sudden, rapid collapse of an algal population, on sediment and water chemistry can only be inferred from studies in the marine environment. Similarly, the role and importance of sediment resuspension and bioturbation in shallow lakes and estuarine environments is fairly well understood and appreciated; yet, comparable 204 J.A. HargreaÕesr Aquaculture 166 (1998) 181–212 information and appreciation is lacking in the aquaculture pond context. As stated previously, practical sediment management will depend on the goals of the culturist: the incorporation of benthivorous fish would favor internal N recycling under conditions of relative N scarcity, while enhancement of bioturbation by the benthos would favor removal processes under conditions of N excess relative to assimilative capacity. The development of imaginative experimental approaches are required to evaluate practical techniques to achieve these goals. 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