Nitrous Oxide (N2O) Emission from Aquaculture: A Review

Critical Review pubs.acs.org/est

Nitrous Oxide (N2O) Emission from Aquaculture: A Review Zhen Hu,† Jae Woo Lee,‡ Kartik Chandran,§ Sungpyo Kim,‡ and Samir Kumar Khanal†,* †

Department of Molecular Biosciences and Bioengineering, University of Hawaii at Manoa, Honolulu, Hawaii 96822, United States Department of Environmental Engineering, College of Science and Technology, Korea University, Yeongi-gun, Chungnam, 339-700, Korea § Department of Earth and Environmental Engineering, Columbia University, United States ‡

S Supporting Information *

ABSTRACT: Nitrous oxide (N2O) is an important greenhouse gas (GHG) which has a global warming potential 310 times that of carbon dioxide (CO2) over a hundred year lifespan. N2O is generated during microbial nitrification and denitrification, which are common in aquaculture systems. To date, few studies have been conducted to quantify N2O emission from aquaculture. Additionally, very little is known with respect to the microbial pathways through which N2O is formed in aquaculture systems. This review suggests that aquaculture can be an important anthropogenic source of N2O emission. The global N2O−N emission from aquaculture in 2009 is estimated to be 9.30 × 1010 g, and will increase to 3.83 × 1011g which could account for 5.72% of anthropogenic N2O−N emission by 2030 if the aquaculture industry continues to increase at the present annual growth rate (about 7.10%). The possible mechanisms and various factors affecting N2O production are summarized, and two possible methods to minimize N2O emission, namely aquaponic and biofloc technology aquaculture, are also discussed. The paper concludes with future research directions. diseases and parasites;11,12 (ii) Fish as an aquatic feed. Farming carnivorous species requires large inputs of wild fish as an aquatic feed, and the capture of these wild fish can affect the aquatic ecosystems indirectly;13,14 (iii) Organic pollution and eutrophication. The discharge of effluent with high concentration of organic matters and nutrients from aquaculture systems to the adjacent water bodies would lead to organic pollution and eutrophication;15−17 (iv) Chemical pollution. A variety of chemicals are used in aquaculture systems as antibiotic resistance substances to curtail the spread of disease;18,19 and (v) Habitat modification. The widespread development of aquaculture industry may endanger mangrove ecosystems.20,21 Another major environmental concern which was not discussed above is associated with release of nitrous oxide (N2O) from microbial nitrification and denitrification within the aquaculture systems. With growing concern of global warming, there is significant effort to quantify the emission of greenhouse gases (GHGs) from anthropogenic sources, such as fuel combustion, agriculture, livestock, etc. GHGs include carbon dioxide (CO2), methane (CH4), N2O, ozone (O3), etc. N2O is the third most important GHG with a global warming potential (GWP) over a 100-year period exceeding 310 times

1. INTRODUCTION Aquaculture is defined as the farming of fish, shellfish, and aquatic plants.1,2 It has been practiced for around 4000 years and is among the fastest-growing segments of the food economy in modern times.3,4 Since the mid-1970s, total aquaculture production has grown significantly, at an average rate of 8.30% per year (1970−2008), and it was recently estimated that aquaculture production in 2009 was 55.10 million metric tons, which accounts for 46.77% of all the fish consumed by humans.5,6 The human demand for protein is increasing, as well as the global population. The Food and Agriculture Organization (FAO) predicted that the human demand for food fish could increase from 16 kg/capita/year in 2006 to 20 kg/capita/year by 2030, raising the total human fish consumption from 72.10 million metric tons to approximately 150 million metric tons.7,8 Since production from capture fisheries has leveled off, aquaculture will play a significant role to meet the increasing demand of aquatic foods. For example, in the United States, an aquaculture policy which called for a “five-fold increase in domestic aquaculture production by the year 2025”, has been underway since 1999.2,9 Although aquaculture can provide a number of benefits such as job creation, improvement of rural economy, and food security, etc., the rapid development of aquaculture also has several environmental concerns. These concerns can be divided into five categories:10 (i) Biological invasion caused by farmed species. The escaped farmed fish may harm wild fish population through competition and interbreeding, or by spreading © 2012 American Chemical Society

Received: Revised: Accepted: Published: 6470

January 10, 2012 May 11, 2012 May 17, 2012 May 17, 2012 dx.doi.org/10.1021/es300110x | Environ. Sci. Technol. 2012, 46, 6470−6480

Environmental Science & Technology

Critical Review

Figure 1. Principal transformation processes of nitrogen in aquaculture system. Assuming a nitrogen input of 1000 gN, and the nitrogen transformation in each pathway is based on statistical analyses of literature published.

11−36%) of the nitrogen consumed can be converted to fish biomass.39−42 Cho et al.43 estimated that approximately 190 g of feces is produced per kg of feed digested. Assuming the nitrogen content of feces as 4%, the nitrogen content of protein in the feed as 16%, about 14% of the nitrogen consumed by fish is wasted as feces.44 The other nitrogen ingested by fish is excreted as un-ionized ammonia, a major product of protein metabolism. In the aqueous phase, ammonia exists in two forms: un-ionized ammonia (NH3), and ionized ammonium (NH4+). The sum of NH4+ and NH3 is usually referred to as total ammonia nitrogen (TAN).45 The relative distribution of each form is primarily a function of pH, temperature and salinity.46 Timmons et al.47 demonstrated that the ammonianitrogen generated per day in an aquaculture system can be estimated using the following equation:

that of CO2. It has a lifetime of 114 years and causes ozone destruction. The concentration of N2O in the atmosphere was reported to be about 322 ppb in 2009.22 Although atmospheric N2O accounts for only 6% of the greenhouse effect, its high increase rate since 1990s (currently 0.25−0.30% per year) has aroused great attention, especially with respect to its sources and sinks.23 Agriculture is considered to be the primary anthropogenic source of N2O emission.24−27 However, most of the studies focus on natural or fertilized soil and few studies have been conducted on N2O emission from aquaculture; also a vital part of agriculture.28−31 Williams and Crutzen32 tentatively estimated that the annual global N2O−N emission from aquaculture in 2008 was 9 × 1010 g, representing 0.51% of global N2O−N emission. Considering the rapid growth rate of aquaculture industry, it is imperative that N2O emissions should be investigated. In this paper, the magnitude and source of N2O emission from aquaculture are reviewed. The paper, however, only focuses on N2O emission within the aquaculture system. The N2O emissions from upstream or downstream processes, such as feed production, fish transportation, etc., are excluded, although they may contribute to a large quantity of GHGs emission.33,34 Operation parameters influencing N2O emission and possible minimization strategies to mitigate its emission are discussed. Finally, further research directions are also included.

PTAN = F × PC × 0.092

(1)

Where PTAN is the production rate of total ammonia nitrogen (kg/day); F is the feeding rate (kg/day); and PC is protein content in feed (in fraction). This equation assumes that protein has a nitrogen content of 16%, 80% of which is assimilated by fish, 80% of the assimilated nitrogen is excreted, and 90% of excreted nitrogen is TAN and the other 10% is urea. Part of the unconsumed feed and feces is removed by sedimentation or filtration, while the dissolved feces and feed are the major contributor to the organic load of aquaculture systems.5 The accumulation of ammonia in aquaculture may impose toxicity to fish. High concentrations of ammonia can decrease survival, inhibit growth, and cause a variety of physiological dysfunctions in fish.48−50 In most cases, the acceptable level of un-ionized ammonia in aquaculture systems is limited to 0.025 mgN/L.51,52 The ammonia in the system can be oxidized to nitrate (NO3−) by nitrifying bacteria under oxic conditions. Nitrate is relatively nontoxic to fish, except at very high concentration (over 300 mgN/L).53 Nitrate is then used as an electron acceptor by denitrifying bacteria under anoxic conditions and is transformed to nitrogen gases (N2 and N2O) that diffuse into the atmosphere. The nitrogen loss as nitrogen gases could account for about 20% of the nitrogen input to the system. In addition, part of the ammonia can escape to atmosphere via volatilization. The ammonia volatilization can be enhanced by increased ammonia concentration, pH, temperature, evaporation rate, and wind speed. But in general it is negligible as a mechanism of nitrogen removal, because the conditions favorable for ammonia volatilization are uncommon in full scale aquaculture systems.39

2. NITROGEN TRANSFORMATION IN AQUACULTURE Nitrogen is a vital chemical component of all living organisms because it is an essential component of deoxyribonucleic acid (DNA), ribonucleic acid (RNA) and protein. Nitrogen transformations are the key biochemical processes in aquaculture systems. Figure 1 shows the principal nitrogen transformation processes in aquaculture systems. About 1 to 3 kg feed (dry weight) is needed to produce 1 kg fish (live weight), depending on the feed conversion ratio.5,14 The major form of nitrogen in the feed is protein. It is necessary to maintain the proportion of protein in the feed at an optimum level to achieve good fish growth. The protein level of fish feed varies from 25 to 55% (35% on average), depending on the cultured species, water temperature, body size, stocking density, etc.1 Part of the feed in aquaculture system (less than 5%) remains unconsumed.14,35−38 The consumed feed is digested by fish, partially converted into fish biomass, partially egested as feces, and partially excreted as un-ionized ammonia through the gills. Results from a variety of aquaculture systems indicated that, on average 25% (range: 6471

dx.doi.org/10.1021/es300110x | Environ. Sci. Technol. 2012, 46, 6470−6480


Critical Review

Table 1. Estimated Fish Production and N2O−N Emission in 2009 and 2030 Species group carps, barbels, cyprinids cods, hakes, haddocks tunas, bonitos, billfishes salmons, trouts, smelts tilapias flatfish river eels sturgeons, paddlefish other fishes shrimp crabs other crustaceans clams, cockles, arkshells oysters mussels scallops abalones, winkles, conchs other mollusks sea urchins, other echinoderms miscellaneous total

Aquaculture production in 2009 (metric ton)a

Average annual growth rate between 1999 and 2009 (%)b

Estimated aquaculture production in 2030 (metric ton)

Estimated N2O−N emission in 2009 (metric ton)

Estimated N2O−N emission in 2030 (metric ton)

22 228 344

4.08

51 477 810

37 566

86 997

22 729

14.39

382 586

38

647

8735

3.22

16 994

15

29

2 458 018

10.91

21 625 685

4154

36 547

3 096 935 169 030 275 159 32 898

5.85 11.48 1.91 26.41

10 219 748 1 656 151 409 389 4 514 187

5234 286 465 56

17 271 2799 692 7629

7 633 908 3 495 972 246 523 1 562 098 4 437 786

7.23 11.95 3.47 16.15 1.51

33 066 585 37 417 434 504 616 36 233 624 6 079 274

12 901 5908 417 2640 7500

55 883 63 235 853 61,235 10,274

4 303 401 1 764 630 1 583 629 546 479

1.49 1.98 5.22 13.69

5 870 838 2 663 599 4 610 178 8 086 137

7273 2982 2676 924

9922 4501 7791 13 666

1 083 156 109 021

−1.58 12.37

775 250 1 262 316

1831 184

1310 2133

622 287 55 058 451

16.72 7.10c

15 997 112 226 872 403

1052 93 048

27 035 383 414

a

Data from published report of Fisheries of the United States on world aquaculture and commercial catches for 2000−2010. bThe average annual growth rate was calculated based on the aquaculture production from 1999 to 2009 (SI Table S3). cData from FAO (2008), the average growth rate between 1995 and 2005.

In aquaculture system, N2O is mainly produced from the microbial nitrification and denitrification, same as in terrestrial or other aquatic ecosystems. Since nitrification and denitrification processes are influenced by many parameters (dissolved oxygen concentration, pH, temperature, etc.), the N2O emission from different aquaculture systems could vary greatly, depending on the environmental conditions. To estimate the global N2O emission, a statistical emission factor is needed. Although there are some studies on natural aquatic ecosystems (such as river, estuary, and ocean), aquaculture, as a man-made ecosystem, more closely resembles biological wastewater treatment systems. The emission of N2O from wastewater treatment systems has been investigated extensively in recent decades.63−67 The N2O emission ratio of wastewater treatment processes also varies greatly in both lab-scale (0−73% of the nitrogen load)68−70 and full-scale (0 to 55% of the nitrogen load).67,71,72 Ahn et al.65 quantified the annual N2O emissions of 12 wastewater treatment plants across the United States and found that the N2O emission can be as high as 1.80% of the influent nitrogen load. A survey of over 80 different kinds of fish species showed that the protein content of fish is 17.72 ± 2.97% (wet body weight) (Supporting Information (SI) Table S1). The nitrogen content of many proteins is around 16%, thus the nitrogen content of fish can be calculated by dividing its protein content by a factor of 6.25.73 The average nitrogen content of fish is then calculated as 2.84%, that is, for every metric ton of harvested fish, about 2.84 × 104 g of feed nitrogen is recovered.

Both TAN and nitrate can be assimilated by heterotrophic bacteria.54,55 As a bonus, for some aquaculture species (e.g., marine shrimp and tilapia), this bacterial biomass produced can be used as an important source of feed protein.55,56 Schneider et al.57 reported that in aquaculture systems the heterotrophic bacteria growth could retain 7% of feed N. The rest of nitrogen is discharged by water exchange. The practice of water exchange is the most effective and widely employed method for maintaining a good water quality. The exchange rate varies from as high as 250% per day for extensive aquaculture to 2 to 10% per day for intensive aquaculture.53,58,59 Nitrogen discharged in the effluents may affect the water quality of the receiving environment.

3. N2O EMISSION FROM AQUACULTURE The microbial conversion of input nitrogen (N) to N2O in soil and aquatic ecosystems is suspected to be the largest sources of global N2O emission.60 A previous study revealed that about one-third of the global anthropogenic N2O emissions are from aquatic ecosystems.61 For rivers and estuaries, about 1.00% of the N input may be converted to N2O, while about 0.75% of N input to streams are emitted to the atmosphere as N2O.60,62 However, to date, very limited research has been conducted to quantify the contribution of aquaculture to the global N2O budget, although it composes a significant part of aquatic production. Here, we argue that aquaculture may be an important source of anthropogenic N2O emission. 6472



Critical Review

Figure 2. Possible pathways of N2O emission in aquaculture systems.

According to former data, about 23.22 ± 5.88% of nitrogen consumed by fish can be converted to fish biomass (SI Table S2).39 Then the total nitrogen consumed by every metric ton of fish is estimated to be 12.23 × 104 g. Assuming that all the feed is ingested by fish (i.e., no unconsumed feed), the nitrogen input to the aqueous phase to produce one metric ton of fish is 9.39 × 104 g. Given a N2O conversion ratio of 1.80%, the amount of nitrogen emitted to atmosphere as N2O−N is 1.69 × 103 g. Thus, the average N2O emission factor of aquaculture system is 1.69 gN2O−N/kg fish. Table 1 shows the estimated fish production and N2O−N emission by species groups in 2009 and 2030. In 2009, the world aquaculture production was 5.51 × 107 metric tons, of which about 40.37% was associated with carp, barbels and cyprinids. The growth rate of different fish species is different. The average annual growth rates of different fish species groups were calculated based on their productions from 1999 to 2009 (SI Table S3). The estimated world aquaculture production in 2030 would be 2.27 × 108 metric tons. Using the emission factor mentioned above, the estimated global N2O−N emission from aquaculture in 2009 and 2030 would be 9.30 × 1010 and 3.83 × 1011 g, respectively. According to the Intergovernmental Panel on Climate Change (IPCC)’s fourth assessment report, the global annual N2O emission is estimated to be about 17.70 × 1012 g N, of which 6.70 × 1012 g N is anthropogenic with a large uncertainty range on each of the individual sources.22,74 Then aquaculture may account for 5.72% of anthropogenic N2O−N emission in 2003. This value is much lower than the result of Williams and Crutzen,32 who estimated that the global N2O−N emissions from aquaculture systems in 2030 would be 1.01 × 1012 g. We believe their results may be overestimated because of the following three reasons: (1) The feed conversion ratio is the ingested feed mass divided by the increased fish mass. Unfortunately, the authors mistakenly used this as the nitrogen conversion rate; (2) Not all the nitrogen in the feed is the “real” nitrogen input. Part of the nitrogen in the feed is assimilated into the fish biomass and does not contribute to N2O production; and (3) It is inaccurate to simply use 8.70% as the global aquaculture growth rate. Different species groups have different growth rates. However, our values may still be overestimated, because the growth rate of aquaculture will slow down with the increase of its production.

detailed insight on nitrogen transformation, especially N2O production is nonexistent.39,75 Due to issues such as difficulties in off-gases collection, and lack of appropriate detection methods, no published literature on the measurement of N2O emissions from aquaculture systems is available. A study on N2O measurement can provide valuable and much needed data to quantify N2O emission from aquaculture. The production of N2O from nitrification and denitrification has long been recognized. However, the exact biochemical mechanism of N2O formation is uncertain and may be attributed to more than one pathway. Figure 2 summarizes the possible biochemical pathways of N2O production in aquaculture systems. 4.1. Denitrification. Denitrification is performed primarily by heterotrophic bacteria. It takes place when oxygen is depleted and nitrate is used as terminal electron acceptor. During denitrification, NO3− is reduced to NO2− by nitrate reductase (Nar), which is then reduced to NO by nitrite reductase (Nir). NO is further reduced to N2O by nitric oxide reductase (Nor) and finally reduced to N2 by nitrous oxide reductase (Nos).76 N2O is one of the obligatory intermediates in complete denitrification. The ratio of N2O/N2 increases if NO3− is abundant because NO3− is a preferred electron acceptor over N2O.77 It is also reported that N2O reductase is more susceptible to oxygen than nitrate and nitrite reductases under low DO concentration. As a result, the N2O reduction rate is lower than the reduction of nitrate and nitrite, leading to a higher N2O/N2 ratio. Despite these, other environmental factors such as temperature,63 pH78 and specific inhibitor (e.g., C2H2),79 as well as the organic electron donor,80 are also reported to influence N2O production through denitrification process. In summary, N2O production through denitrification can be enhanced by low oxygen level, sufficient NO3− and biodegradable organic carbon, low pH and temperature, and specific inhibitor. 4.2. Autotrophic Nitrification. Nitrification is carried out by two groups of autotrophic microorganisms: ammoniaoxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB). Ammonia is first oxidized to nitrite by AOB and then converted to nitrate by NOB.81 Some intermediates are produced during autotrophic nitrification, e.g. hydroxylamine (NH2OH). The oxidation of NH4+ to NH2OH is catalyzed by ammonia monooxygenase (AMO).82 The next step in NH4+ oxidation is from NH2OH to NO2−, which is catalyzed by hydroxylamine oxidoreductase (HAO).83 The NO2− produced is further oxidized to NO3− in a one-step reaction under the catalytic effect of nitrite oxidoreductase (NOR).81

4. POTENTIAL SOURCES OF N2O IN AQUACULTURE Figure 1 shows the nitrogen transformation processes in aquaculture systems. Several studies have been conducted to exam the nitrogen balance of aquaculture systems, however, a 6473



Critical Review

In general, autotrophic nitrification, denitrification, nitrifier denitrification, and coupled nitrification and denitrification may all contribute to N2O emissions from aquaculture systems. However, the exact emission mechanisms are related to the specific operating parameters and environmental conditions, and there is little published literature available to distinguish the contribution of each pathway. Further research is needed.

N2O can be formed during ammonia oxidation through chemical decomposition of intermediates from the oxidation of NH4+ to NO2− or of NO2− itself with organic (e.g., amines) or inorganic (e.g., Fe2+ or Cu2+) compounds.84 This is usually regarded as a special form of chemodenitrification.85 However, this chemical process is reported to occur only when the NO2− concentration is relatively high (>1 mM).86 Since NO2− is toxic to aquatic species, the concentration of NO2− in a mature aquaculture system should not exceed 10 mg/L for a long period and in most cases is maintained below 1 mg/L.53 The chemodenitrification may not be a significant pathway of N2O production in aquaculture systems. In addition, there is also evidence that N2O can be produced through the aerobic hydroxylamine oxidation pathway. Hydroxylamine generated during ammonia oxidation is oxidized to NO directly under the catalysis of enzyme HAO encoded by the haoAB genes,87 and then reduced to N2O under the catalysis of c554 cytochrome (Cyt c554).88 Several studies using the stable isotopic composition of N2O suggested that N2O in oxic waters is mainly from nitrification.62,89,90 Furthermore, IPCC also assumes that nitrification produces twice as much N2O emission as denitrification in streams and rivers.60 Thus the aerobic hydroxylamine oxidation pathway of nitrification process may play an important role in N2O emission from aquaculture systems. 4.3. Nitrifier Denitrification. For a long time, nitrification was considered to be carried out by autotrophic bacteria while denitrification was thought to be conducted by heterotrophic bacteria. However, as a result of imbalance between total input and output of N in many environments, there is now a renewed interest in better elucidating nitrifier denitrification. In nitrifier denitrification, the oxidation of NH3 to NO2− is followed by the reduction of NO2− to N2O. This sequence of reactions is carried out by only one group of microorganisms, namely autotrophic ammonia-oxidizing bacteria. The first part of nitrifier denitrification (NH3 to NO2−) has been attributed to nitrification (NH3 oxidation). The second part, the reduction of NO2−, is regarded as denitrification. All the enzymes required to carry out nitrifier denitrification are believed to be essentially the same as for ammonia oxidation and denitrification.84 Nitrifier denitrification is considered to be responsible for most of the N2O emissions from wastewater treatment processes.64,91 As mentioned above, the aquaculture system resembles biological wastewater treatment system. Thus, nitrifier denitrification may also play a significant role in N2O emissions from aquaculture systems. 4.4. Coupled Nitrification and Denitrification. Coupled nitrification and denitrification is actually not a separate process; but a combination of nitrification and denitrification. In this process, the NO2− or NO3− produced through nitrification is reduced to N2O or N2 by denitrifiers directly. This process usually takes place in environments where favorable conditions for both nitrification and denitrification are present in neighboring microhabitats. Previous studies showed that high quantities of N2O can be produced under conditions that are suboptimal for both nitrifiers and denitrifiers.92−94 In aquaculture systems, the oxic and anoxic zones can coexist in the nonturbulent area or inside the biofloc,95 where the conditions are more favorable for the occurrence of the coupled nitrification and denitrification. Thus coupled nitrification and denitrification may also contribute to the N2O emissions from aquaculture systems.

5. FACTORS INFLUENCING N2O EMISSION N2O emissions are closely related to the activities of the nitrifiers and denitrifiers, which are influenced by environmental factors, such as DO, pH, salinity and availability of substrate. The detailed discussion on important factors affecting N2O emissions from aquaculture is presented in the following section. 5.1. Feed Type and Feeding Rate. Feed type and feeding rate affect ammonia concentration in the aqueous phase. According to eq 1, the TAN production of aquaculture correlates with the feeding rate and protein content in the feed. Cole and Boyd96 reported a strong correlation between the daily feeding rates and the concentration of TAN in a Channel catfish (Ictalurus punctatus) pond. A recent study revealed a positive correlation between the ammonia concentration and nitrification-driven N2O emission in pure cultured Nitrosomonas europaea, the best studied autotrophic ammonia-oxidizing bacterium.97 Higher ammonia concentration, resulting from higher feeding rate, can increase the specific activity of N. europaea, thus leading to a higher autotrophic production rate of N2O. 5.2. Water Exchange Rate. Water exchange is the most effective and commonly used method to maintain good water quality in aquaculture system. The rate of water exchange can affect the concentrations of nitrogen compounds in aquaculture systems. Lorenzen et al.98 studied the effect of water exchange on semi-intensive shrimp ponds, and results showed that ammonia concentration was minimal with no water exchange, increased to a maximum value at water exchange rates of 20− 40% turnover per day, and decreased at water exchange rates exceeding 40% turnover per day. This may be related to the balance between the removal of ammonia and wash-out of nitrifiers by water exchange. Lower concentrations of nitrogen compounds, as well as decrease in nitrifiers’ population, will lead to less N2O emission. Thus, water exchange rate impacts the N2O emission indirectly. In addition, it should be noted that reduced exchange and nonexchange treatments could result in reduced environmental impacts to surrounding water bodies.99 5.3. DO Concentration. Optimum DO concentration in the aqueous phase is essential for both fish growth and nitrifier activity. Theoretically, DO concentrations should be maintained above 5.0 mg/L for optimum fish growth in aquaculture systems.53 To achieve such high DO concentrations, intensive and continuous aeration is required. However, studies have shown that intense aeration for maximum fish production is less profitable than moderate aeration to improve water quality and to enhance feed conversion ratio.95 In addition, in an aquaculture system, there exist anoxic zones with low mixing and low DO concentrations. Oxygen limitation, usually caused by insufficient aeration or mass transfer limitation in large bioflocs, is a well-known trigger of N2O production.66,94 During nitrification, autotrophic ammonia oxidizers use nitrite as the terminal electron acceptor in oxygen limiting conditions; thus increasing N2O production 6474



Critical Review

(Salmo salar) is around 17 °C.108 At temperatures lower than optimum, growth rates, feed consumption rates and metabolic activities of fish are reduced significantly; whereas elevated temperature correlates well with increase growth rate up to an optimum point beyond which thermal stress occurs.109,110 The optimum temperature for nitrification and denitrification process is between 25 and 30 °C, and both the processes are inhibited at temperature of 10 °C or lower.111,112 Temperature affects N2O emission by affecting the overall nitrification and denitrification processes. Hu et al.63 investigated the effect of temperature on N2O emission from wastewater treatment process and higher N2O fluxes was found at lower temperatures (temperature range: 15−35 °C), mainly because low temperature affects N2O reductase to a greater extent than the N2O producing enzymes (NO3−, NO2− and NO reductase).113 Significant decrease in N2O emission was found when temperature was lower than 10 °C, probably because of the inhibition effect of low temperature. Besides, N2O has a higher solubility at low temperature.114 The dissolved N2O is less likely to be released to atmosphere due to air stripping. 5.7. Salinity. In aquaculture systems, especially with high stocking density, various forms of nitrogen (NH4+, NO2−, NO3−, etc.) accumulates with feed addition. In addition, salt (e.g., NaCl) is usually added to the system to block nitrite toxicity and relieve osmotic stress.53 A salt concentration of 0.20 to 2.00 mg/L is beneficial for most species of fish and invertebrates. In 2009, about 60.40% of world aquaculture production was from fresh water, while marine and brackish water, respectively account for 31.70% and 7.90% of world aquaculture production.115 High salinity can influence N2O emission both directly and indirectly via the inhibition of N2O reductase activity. Tsuneda et al.116 reported an increase of N2O conversion rates from 0.22% to 0.48% when the salt concentration increased from 10 to 20 mg/L in the single nitrification process, while no significant change in N2O conversion was observed when the salt concentration increased from 30 to 50 mg/L in the single denitrification process. Other studies on coastal water revealed a negative relationship between salinity of dissolved N2O concentration.117,118 5.8. Toxic Compounds. In aquaculture systems, if anaerobic conditions prevail at the bottom, hydrogen sulfide (H2S) can be generated through biological sulfate reduction.119,120 This may result in the mass mortality of the fish.121 Unionized H2S is also inhibitory to N2O reductase enzymes. Schonharting et al.122 reported that H2S concentrations above 0.32 mg/L can significantly inhibit the activity of N2O reductase and hence result in high N2O emissions.

through aerobic hydroxylamine oxidation pathway and nitrifier denitrification pathway. During denitrification, the synthesis and activity of all denitrification enzymes are inhibited in the presence of oxygen. Since N2O reductase is more sensitive to oxygen than the other enzymes,100 large amount of N2O can be produced through denitrification under low DO conditions. However, because N2O has a relatively high solubility in water (Henry coefficient, 0.024 L·atm/mol),101 air stripping also has significant effect on N2O emission. Low DO concentration, if caused by insufficient aeration, may also lead to less N2O emission because of low air stripping. 5.4. Cultured Species. A large variety of aquatic animals can emit N2O when nitrate is present in the environment. This is attributed to incomplete denitrification by ingested bacteria in the anoxic animal gut. Stief et al.31 found that the N2O emission rate is correlated to the feeding guild to which the species belonged to. Filter- and depositfeeding animal species showed the highest rate of N2O emission while predators had the lowest. This is probably because the filter- and depositfeeding species ingest greater number of microbes than other species.102 Heisterkamp et al.103 also investigated the N2O emission from 19 different invertebrate species and the results showed that marine invertebrates can emit N2O at substantial rates. The potential N2O emission rates of the invertebrate species investigated ranged from 0.00 to 1.35 nmol/(individual · h). A much higher N2O emission rate (3.57 nmol/ (individual·h)) was found in aquacultured shrimp (Litopenaeus vannamei), probably due to the high nitrate concentrations in the rearing tanks. In 2009, the world aquacultured shrimp production was 3.50 × 106 metric tons (SI Table S3). Assuming that the average weight of harvested shrimp as 25.00 g and the average production cycle of 25 weeks,104 N2O−N produced by shrimp would be around 1.65 × 107 g. This accounted about 0.018% of total N2O emission from aquaculture. Although shrimp production only accounts for 6.35% of world aquaculture production, it is still logical to infer that aquatic animals only contribute to a small fraction of total N2O emission from aquaculture systems. 5.5. pH. Fish can tolerate a pH ranging from 6.00 to 9.50. There is also evidence that fish can live well even at an acidic pH of around 4.00. However, the optimum pH ranges for aquaculture system are between 7.00 and 8.00. Higher or lower pHs may increase the mortality.105 The pH of an aquaculture system tends to decline as the nitrification process produces hydrogen ions which consume alkalinity. Furthermore, the generation of carbon dioxide by the fish and microorganisms also decrease alkalinity. To maintain the optimum pH range, alkalinity supplementation chemicals, such as sodium bicarbonate and calcium carbonate must be added at a rate of 17− 20% of the daily feeding rate.53 The pH significantly influences the activity of enzymes during nitrification and denitrification; thus affects the production of N2O. While neutral pH is optimum for both nitrification and denitrification, N2O production by AOB increased with the increase of pH,106 and the denitrificationdriven N2O production increased with the decrease of pH.69 5.6. Water Temperature. Water temperature is one of the critical parameters for successful operation of an aquaculture system. Different species require different temperature. The optimum temperature for the growth of Channel catfish (Ictalurus punctatus) fingerlings is between 26 and 32 °C,107 while the optimum temperature for growth of Atlantic salmon

6. POTENTIAL WAYS TO REDUCE N2O EMISSION FROM AQUACULTURE In an earlier section (Section 3) we discussed that aquaculture may account for 5.72% of anthropogenic N2O−N emission in 2003. Although the fraction is relatively low compared with fertilized soil, considering the high global warming potential of N2O, it is important to study the minimization strategies of N2O emission from aquaculture. In addition, low N2O production can be an indication of stable nitrification and denitrification.97,123 In this case, the concentration of NH4+ and NO2− is low, which is ideal for fish growth. The most common method to control N2O emission from aquaculture is to keep the system under optimal operating conditions, such as appropriate pH and temperature, sufficient 6475



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heterotrophic bacteria can assimilate the inorganic nitrogen accumulated in aquaculture system, thus reduce their concentrations and lead to a lower N2O production. Although BFT may minimize N2O emission from aquaculture system, the addition of carbohydrate substrates can enhance its production of CO2 at the same time. Assuming a feed protein content of 35%, for 1 kg feed, about 233 g of carbohydrate addition is need to conduct BFT, according to the theory provided by Yoram.54 Since the carbon content of added carbohydrate is roughly 50% and about 50% of the organic carbon is converted to CO2, the increase of CO2 caused by carbohydrate addition is 425 g.54 And based on the calculation in Section 3, in aquaculture system approximately 1.20 g N2O could be emitted per kg feed digested, which has a GWP equivalent to 372 g CO2. Therefore, even if all the N2O emission from aquaculture system can be minimized by BFT, it may still increase the total greenhouse gases emission when taking CO2 into consideration. However, it has been reported that the application of BFT can increase the shrimp production and protein utilization rate by 50% and 20%, respectively.133 Detailed research and cost-effective analysis are needed to evaluate the effect of BFT on minimizing greenhouse gases emission.

DO, good quality feed, etc. Furthermore, the improvement in the design of aquaculture system could be a promising alternative. Two potential ways to minimize N2O emissions from aquaculture systems are discussed here. 6.1. Aquaponic Aquaculture. Aquaponic aquaculture is a special form of recirculating aquaculture systems (RAS), namely a polyculture consisting of fish tanks (aquaculture) and plants which are cultivated in the same water cycle (hydroponic).124 The essential components of an aquaponic system are the fish-rearing tank, solid removal component, hydroponic component, and sump. The schematic diagram of an aquaponic aquaculture system is shown in SI Figure S1. Effluent from the fish-rearing tank is first treated with a solid removal component to reduce settleable and suspended solids. Ammonia and nitrate in the water are then removed through a hydroponic unit where nitrification and denitrification occur and dissolved nutrients are taken up by the plants. Finally, the water is collected in a sump and is recycled into the fish-rearing tank.125 The plant used in the hydroponic component depends on the stocking density of fish tanks and subsequent nutrient concentration of aquaculture effluent.126 Because of its high efficiency and eco-friendly nature, aquaponic aquaculture has generated great interest in recent years. It is likely to be one of the widely accepted methods of food production in the future. Theoretically, in order to ensure optimal plant growth and photosynthesis, the surface area of hydroponic component is kept twice that of fish-rearing tank.124 Compared with traditional recirculating aquaculture systems, aquaponic aquaculture system has a larger nutrient recycling capacity and thus minimizes the concentration of NH4+, NO2− or NO3−. In addition, plant growth can also assimilate part of ammonia and nitrate in the system. Sfetcu et al.127 compared the conventional recirculating aquaculture system with aquaponic recirculating aquaculture system. The latter system demonstrated lower concentrations of NH4+, NO2− and NO3−, all of which led to less N2O emissions. However, there is a concern that plants in the hydroponic component can also contribute to the emission of N2O.128,129 Further research is needed to evaluate N2O emissions from aquaculture-aquaponic systems. 6.2. Bioflocs Technology (BFT) Aquaculture. BFT aquaculture is developing and controlling heterotrophic bacteria in flocs within the fish culture component. The system is developed based on the knowledge of conventional domestic wastewater treatment systems and is conducted by adding carbohydrates.54,130 By adding carbohydrate substrates to the system, the growth of heterotrophic bacteria is stimulated and nitrogen uptake through the production of microbial proteins take place.131 The resulting heterotrophic biomass can be utilized as a food source by fishes and invertebrates. The BFT aquaculture is one of the approaches developed to make the aquaculture industry sustainable through (1) increasing nitrogen retention in the harvested target biomass, (2) reducing the demand for feed protein, (3) reducing the concentration of potentially toxic TAN and NO2− in the system, and (4) reducing the nitrogen discharged into the environment. Because of its sustainability attributes, the bioflocs technology will certainly play an extremely important role in the future of the aquaculture industry. Since the growth rate and microbial biomass yield per unit substrate of the heterotrophic bacteria are higher than the nitrifiers, the nitrifiers could be outcompeted by heterotrophic bacteria after a long-term acclimation.132 This will decrease the nitrification-driven N2O production. In addition, the growth of

7. FUTURE RESEARCH DIRECTIONS Considering the high global warming potential of N2O, even miniscule quantities of N2O emissions from aquaculture systems are unwanted. Peer-reviewed publications cited provide valuable insights into nitrogen transformation in aquaculture systems; however, most studies focused on the nitrogen retention in the harvested target biomass. To date, no published research on the measurement of N2O emissions from aquaculture systems is available. There is a critical need to quantify N2O emissions from aquaculture systems and mitigate its impact on global climate change. In addition, due to lack of precise measurement techniques, large spatial variability, seasonal and climate variability, a national inventory of N2O emission from aquaculture is difficult to establish. It is essential to develop appropriate simulation models to estimate the N2O emission over a number of seasons and areas to better represent the impact that increasing aquaculture practices may have in the near- and far-term future. Although the biochemical mechanisms of N2O production in soils, wastewater treatment plants and some aquatic environments have been extensively studied, a comprehensive understanding of the production mechanisms of N2O in aquaculture system, as well as the contribution of each process to N2O emission, is not readily available. The combined use of stable isotope and chemical inhibition techniques may be able to provide useful information on sources of N2O in aquaculture system. Finally, the introduction of molecular techniques will enable the study of N2O emissions from a fundamental point of view.

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ASSOCIATED CONTENT

S Supporting Information *

Additional material as noted in the text. This material is available free of charge via the Internet at http://pubs.acs.org. 6476



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Corresponding Author

*Phone: 1-808-956-3812; fax: 1-808-956-3542; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work is supported by National Research Foundation Grant funded by the Korean Government (NRF-2011-220D00071) and Supplemental Research and Extension Grant from the College of Tropical Agriculture and Human Resources (CTAHR), University of Hawaii at Manoa. We thank the three anonymous reviewers for their critical comments and helpful suggestions that improved the quality of this paper greatly.

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Nitrous Oxide (N2O) Emission from Aquaculture: A Review

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