Development of water quality criteria of ammonia for protecting aquatic life in freshwater using species sensitivity distribution method

Science of the Total Environment 634 (2018) 934–940

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Development of water quality criteria of ammonia for protecting aquatic life in freshwater using species sensitivity distribution method Tae-Jin Park a,b, Jong-Hyeon Lee c, Myung-Sung Lee a, Chang-Hee Park a, Chang-Hoon Lee c, Seong-Dae Moon d, Jiwoong Chung c, Rongxue Cui e, Youn-Joo An e, Dong-Hyuk Yeom f, Soo-Hyung Lee a, Jae-Kwan Lee a, Kyung-Duk Zoh b,⁎ a Water Environmental Engineering Research Division, National Institute of Environmental Research, Environmental Research Complex, Hwangyeong-ro 42, Seo-gu, Incheon 22689, Republic of Korea b Department of Environmental Health Science, Graduate School of Public Health, Seoul National University, 1 Gwanakgu, Seoul 08826, Republic of Korea c EH R&C, 114, A-dong, Environmental Industry Research Park, Jeongseojin-ro 410, Incheon 22689, Republic of Korea d Neoenbiz, 187-7 Dodang-dong, Buchon-si, Gyeongi-do 14523, Republic of Korea e Department of Environmental Health Science, Konkuk University, 120 Neungdong-ro, Gwangjin-gu, Seoul 05029, Republic of Korea f Korea Institute of Toxicology, 17, Jegok-gil, Munsan-eup, Jinju-si, Gyeongsangnam-do 52834, Republic of Korea

H I G H L I G H T S

G R A P H I C A L

A B S T R A C T

• The species sensitivity distribution (SSD) method was used for ammonia guideline. • Acanthocyclops vernalis and Daphnia galeata were the most sensitive in the SSD. • The guideline for ammonia was found to be 22 mg/L at pH 7 and 20 °C. • 0.09–0.51% of monitoring data in rivers and lakes in Korea exceeded this guideline. • Our results can provide the basis for introducing the ammonia standard in Korea.

a r t i c l e

i n f o

Article history: Received 12 January 2018 Received in revised form 31 March 2018 Accepted 1 April 2018 Available online xxxx Editor: D. Wunderlin Keywords: Total ammonia nitrogen Aquatic life Ecological risk assessment Water quality criteria Species sensitivity distribution HC5 value

⁎ Corresponding author. E-mail address: [email protected]. (K.-D. Zoh).

https://doi.org/10.1016/j.scitotenv.2018.04.018 0048-9697/© 2018 Elsevier B.V. All rights reserved.

a b s t r a c t Ammonia is deemed one of the most important pollutants in the freshwater environment because of its highly toxic nature and ubiquity in surface water. This study thus aims to derive the criteria for ammonia in freshwater to protect aquatic life because there are no water quality criteria for ammonia in Korea. Short-term lethal tests were conducted to perform the species sensitivity distribution (SSD) method. This method is widely used in ecological risk assessment to determine the chemical concentrations to protect aquatic species. Based on the species sensitivity distribution method using Korean indigenous aquatic biota, the hazardous concentration for 5% of biological species (HC5) value calculated in this study was 44 mg/L as total ammonia nitrogen (TAN). The value of the assessment factor was set at 2. Consequently, the criteria for ammonia were derived as 22 mg/L at pH 7 and 20 °C. When the derived value was applied to the monitoring data nationwide, 0.51%, 0.09%, 0.18%, 0.20%, and 0.35% of the monitoring sites in Han River, Nakdong River, Geum River, Youngsan River, and lakes throughout the nation, respectively, exceeded this criteria. The Ministry of Environment in Korea has been considering introducing water quality standard of ammonia for protecting aquatic life. Therefore, our results can provide the basis for introducing the ammonia standard in Korea. © 2018 Elsevier B.V. All rights reserved.

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Table 1 Characteristics of Korean native aquatic species in laboratory toxicity tests with different total ammonia nitrogen (TAN) concentrations. Scientific name

Taxonomic grouping

Source

pH

Measured concentration of TAN (mg/L)

Aphyocypris chinensis

Fish

Hatchery

Pomacea canaliculata

Mollusca

Stream

Daphnia galeata

Cladocera

Laboratory culture

Rana huanrenensis Gammarus sobaegensis Acanthocyclops vernalis Chironomus kiiensis Brachionus calyciflorus Branchinella kugenumaensis

Amphibian Amphipoda Copepoda Diptera Rotifera Amphipoda

Valley Valley Stream Stream Stream Stream

6.5 7.2 8.0 6.4 7.0 7.8 7.2 7.6 8.0 7.3 7.8 7.7 7.2 7.7 7.6

1.02, 28.8, 117, 234, 466, 978 1.66, 54.9, 112, 229, 390, 770 1.21, 3.38, 9.62, 20.7, 36.0,72.1 0.100, 26.6, 69.7, 126, 280, 611 0.100, 7.24, 15.1, 32.4, 69.3, 137 0.100, 2.45, 5.58, 13.4, 30.5, 60.7 0.100, 19.2, 33.0, 64.0, 69.0, 94.3 0.100, 12.1, 29.9, 41.4, 58.2, 77.4 0.100, 10.9, 19.0, 26.0, 32.9 0.450, 58.2, 66.8, 200, 269, 344 0.100, 3.70, 6.46, 17.9, 37.6, 80.2 0.100, 10.4, 17.0, 44.6, 91.8 3.88, 322, 574, 1051, 1910, 3499 0.100, 14.1, 29.1, 67.8, 151, 238, 498 0.0259, 20.0, 42.5, 86.0, 184, 369

1. Introduction Ammonia was included in the second Priority Substances List pursuant to the Canadian Environmental Protection Act, 1999 (Minister's Expert Advisory Panel 1995) due to the concerns about its harmful effects on organisms exposed to significant levels of ammonia released from various anthropogenic and natural sources (Constable et al., 2003). The anthropogenic sources of ammonia in the aquatic environment include municipal effluent discharges and agricultural runoff and the natural sources include nitrogen fixation and the excretion of nitrogenous waste from animals (US EPA, 2013). The chemical form of ammonia in water comprises two species, the more abundant one is the ammonium ion (NH+ 4 ) and the less abundant one is the non-dissociated or unionized ion molecule (NH3). The ratio of

these species in a given aqueous solution depends on both pH and the temperature of the water; as pH and temperature increase, the concentration of NH3 also increases but the concentration of NH+ 4 decreases (Emerson et al., 1975). The concentration of total ammonia is the sum of NH+ 4 and NH3 concentrations (US EPA, 2013). The ionized ammonium ion and unionized ammonia molecule are interrelated through the chemical equilibrium between NH+ 4 and NH3 (Emerson et al., 1975). The unionized ammonia is very toxic to aquatic life, particularly to fish, whereas ionized ammonia is nontoxic or significantly less toxic (Russo, 1985; Environment Canada, 2001). Toxic effects of ammonia on aquatic life have been extensively studied. In fish, for example, ammonia can cause proliferation in gill tissues, increase ventilation rates, damage the gill epithelium (Lang et al., 1987), reduce blood oxygen-carrying capacity due to progressive acidosis

Fig. 1. Map of four major river basins in Korea, in which there are 905 monitoring stations nationwide.

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Fig. 2. Comparison of toxicity of total ammonia nitrogen (TAN) before (left) and after (right) the adjustment at pH 7 and 20 °C.

(Russo, 1985), and uncouple oxidative phosphorylation inhibiting production and depletion of adenosine triphosphate (ATP) in the brain (Camargo and Alonso, 2006). To protect freshwater ecosystems from the toxicity of ammonia, a number of criteria or criteria have been established around the world. For instance, the United Sates Environment Protection Agency (US EPA) set acute water quality criteria at 17 mg/L for total ammonia nitrogen at pH 7.0 and 20 °C (US EPA, 2013). Canada recommended a water quality criteria for NH3 at 19 μg L−1 NH3, which was derived from chronic toxicity data (CCME, 2010). Australia and New Zealand governments jointly recommended the water quality criteria of 30 μg L−1 NH3 at pH 8.0 to protect 95% of freshwater species (ANZECC and ARMCANZ, 2000). However, Korea has no recommended water quality criteria for ammonia to protect aquatic life in freshwater ecosystems. As a result, since 2014, a number of studies have been conducted to derive the value that is safe for Korean indigenous aquatic species using the species sensitivity distribution (SSD) method. Species sensitivity distributions are useful for comparing the sensitivities of different groups of organisms (Brix et al., 2001) and are frequently used in ecological risk assessments for the formulation of water quality criteria (Hose, 2005). The main goal of SSDs is to determine the concentration of a toxicant to protect most species (usually 95%) in the environment. SSDs are constructed by fitting a cumulative distribution function to a plot the species toxicity data against rank-assigned percentiles (Koojiman, 1987; Wheeler et al., 2002). This study has three main objectives: (1) to determine whether the equation developed by US EPA (2013) is applicable to derive the criteria for ammonia for freshwater ecosystems in Korea; (2) to determine the concentration of total ammonia nitrogen (TAN) as a criteria to protect aquatic life using SSDs using Korean indigenous aquatic biota; and (3) to identify the number of sites exceeding this criteria by applying the derived criteria to the monitoring data from rivers and lakes nationwide.

Korean taxonomic groups. These include insects (Chironomus kiiensis), amphibian (Rana huanrenensis), fish (Aphyocypris chinensis), mullusca (Pomacea canaliculata), crustaceans (Gammarus sabaegensis, Acanthocyclops vernalis, Branchinella kugenumaensis, Daphnia galeata), and rotifer (Brachionus calyciflorus). All the organisms tested in this research were obtained from different places. For example, R. huanrenensis and G. sabaegensis were obtained in a valley located in the eastern part of Gyeonggido, while B. kugenumaensis was acquired in a stream located in Gyeongsangbukdo. A. chinensis was obtained through subculture at the Korea Institute of Toxicology, Gyeongsangnamedo. Daphnia galeata was acquired through subculture at the Environmental Toxicity Laboratory of Kon Kuk University. C. kiiensis, B. calyciflorus, and A. vernalis were obtained in a stream near EH R&C in Incheon. P. canaliculata was acquired in Chungcheongbukdo. Before toxicity tests were carried out, all the tested organisms were acclimated to general test conditions for a minimum of four days, during which no food was provided.

2. Materials and methods

Regional differences may cause variations in the chemical components and physical characteristics of water bodies, which, in turn, affect the sensitivity of aquatic life (Gao et al., 2014). Therefore, we need to ascertain whether a model or an equation developed for one country is applicable to another country before the model or the equation is used to establish water quality criteria. We verified the applicability of the equation developed by US EPA (2013) to Korea's aquatic environment

2.1. Test chemicals and test organisms Ammonium chloride, (NH4Cl, N99.5% purity) was acquired from Wako, Japan. Short-term lethal exposure tests for ammonia were conducted with different aquatic organisms belonging to six different

2.2. Chemical analysis Toxicity to aquatic organisms is mostly related to ammonia, rather than ammonium, but laboratory tests measured total ammonia. Total ammonia nitrogen (TAN) of tested water samples was analyzed by strictly following the Korean standard methods provided by the Korean Ministry of Environment (2017). Before and after toxicity tests were carried out; the treated samples were measured to determine the medium lethal concentration (LC50) accurately. Geometric mean was used in this toxicity tests. The concentrations of TAN in water samples were determined using the Indophenol method. 2.3. Verification of fitness of the equation

Table 2 Difference in minimum and maximum LC50 of total ammonia nitrogen (TAN) in Korean three native species before and after the adjustment at pH 7 and 20 °C. Scientific name

LC50 before the adjustment of pH and temperature (mg TAN/L) Minimum

Maximum

Aphyocypris chinensis Pomacea canaliculata Daphnia galeata

44.5 15.8 14.4

282 95.0 40.3

LC50 difference (times)

LC50 after the adjustment of pH and temperature (mg TAN/L) Minimum

Maximum

6.3 6.0 2.8

207 78.8 53.4

304 92.5 67.4

LC50 difference (times)

1.5 1.2 1.3

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Table 3 LC50 of total ammonia nitrogen (TAN) in nine species before and after the adjustment of pH and temperature. Scientific name

Taxonomic grouping

pH

Temperature

LC50

LC50 after pH and temperature adjusted

Brachionus calyciflorus Acanthocyclops vernalis Daphnia galeata Branchinella kugenumaensis Gammarus sobaegensis Chironomus kiiensis Pomacea canaliculata Rana huanrenensis Aphyocypris chinensis

Rotifera Copepoda Cladocera Amphipoda Amphipoda Diptera Mullusca Amphibian Fish

7.7 7.7 7.2 7.6 7.8 7.2 7.3 7.3 7.3

23 23 21 23 23 23 23 20 23

266 11.7 40.3 121 24.5 445 47.8 116 146

886 37.6 53.4 311 95.5 685 82.3 172 268

using three Korean native aquatic species (A. chinensis, P. canaliculata, and D. galeata). Toxicity tests on each species were performed depending on different pH values and ammonia concentrations. After we derived LC50 from the tests with these three species, we compared the differences in LC50 values before and after pH and temperature values were adjusted. We used the Eq. (1) below from US EPA (2013) to convert total ammonia nitrogen (TAN) to TAN adjusted at pH 7 and 20 °C. 0 B logA ¼ logB @

1 TAN 0:0114

1 þ 107:204−pH

þ

1:6181

C C−½−0:036ðT−20Þ ð1Þ A

1 þ 10pH−7:204

where [TAN] is the concentration of total ammonia nitrogen; T is temperature (°C), and A is the concentration of TAN adjusted at pH 7 and 20 °C. 2.4. Aquatic animal exposure tests Static non-renewal experimental methods were employed for shortterm lethal tests. The duration of toxicity tests varied with species type. The duration of toxicity tests for R. huanrenensis, G. sabaegensis, C. kiiensis, P. canaliculata, and A. chinensis was ≤96 h; for A. vernalis, B. calyciflorus and B. kugenumaensis ≤24 h; and for D. galeata ≤48 h. Test solutions were not changed during the test period. The concentrations listed in Table 1 were used for lethal tests. For exposure tests to all organisms (except for D. galeata), each concentration contained ten organisms. Depending on the species, the number of replicates was different. For A. vernalis, each concentration was 5 replicates while the tests for B. calyciflorus and A. chinensis were 3 replicates. For D. galeata toxicity test, each concentration contained five organisms and was 3 replicates. Dead organisms were recorded twice a day and removed from experimental vessels. Experiments were conducted under a light-dark cycle for 16 h; 8 h with the light intensity (10–20 μE/m2/s) in a temperature-controlled room in 600-mL glass beakers for macroinvertebrates and 20-L glass tanks for fish. Water quality parameters, including pH, dissolved oxygen (DO) and temperature, were measured at the beginning and at the end of the experiment. Mortality was evaluated in different ways for different species. In general, animals were considered dead when they did not respond to any form of repeated tactile stimulation using a plastic pipette after 10 s under a stereomicroscope (Van Wijngaarden et al., 2010). The mortality score endpoints for short-term exposure tests were used to calculate the median lethal concentrations (LC50). Mortality of organisms in controls was b10% for all exposure tests in short-term tests (Mensah et al., 2013). 2.5. Calculation of HC5 and PNEC The main purpose of the analysis with SSD is to determine hazardous concentrations (HCs) to protect most of the species in the environment (Gao et al., 2014). HCs are calculated by assuming a statistical distribution, for instance, log-normal or log-logistic distribution, of species sensitivities expressed as median lethal concentration (LC50) or median

effective concentration (EC50) values. Therefore, HCs are developed as an analytical expression for the concentrations associated with the pth percentile of the distribution, also referred to as the HC for p percent of the species (Koojiman, 1987; Van Straalen and Denneman, 1989). For example, the HC5 (hazardous concentration for 5% of species) is the estimated the fifth percentile of the distribution, i.e., the concentration expected to protect the 95% of the species in an ecosystem (Wheeler et al., 2002). In this study, only one method (a log-normal distribution) was used to make the comparisons feasible and statistically meaningful since this distribution often fits the toxicity data well (Koojiman, 1987; Newman et al., 2000; Wheeler et al., 2002; Feng et al., 2012). Species sensitivity distributions and the hazardous concentrations at 5% (HC5 value) were estimated using a log-normal distribution (Eq. (2)) in the software ETX 2.0 (Wintersen et al., 2004); 1  y¼ ðP 1−x Þ 1 þ exp p2

ð2Þ

where y is the cumulative probability of species, defined as (the order of the data point) / (1 + total number of data points), x is the mean of the log10-transformed LC50 values, P1 is the parameter representing the intercept, and P2 is the parameter representing the slope of the curve (Wang et al., 2014). Only LC50 values were used to calculate SSDs and HC5 values because LC50 was one of the most frequently reported endpoints. SSDs were generated using the geometric mean of LC50 values for each species. Predicted no effect concentration (PNEC) values are usually derived from a statistical cutoff value of 5% for p. This value of 5% is a practical choice but has been validated based on the field studies (Posthuma et al., 2002). According to the assessment factor method

Table 4 Genus Mean Acute Value (GMAV) of total ammonia nitrogen (TAN). Scientific name

GMAV at pH 7 and 20 °C (mg TAN/L)

Reference

Acanthocyclops vernalis Aphyocypris chinensis Brachionus calyciflorus Branchinella kugenumaensis Ceriodaphnia dubia Chironomus kiiensis Chydorus sphaericus Cyprinus carpio Daphnia galeata Gammarus sobaegensis Gasterosteus aculeatus Lepomis macrochirus Limnodrilus hoffmeisteri Lumbriculus variegatus Micropterus salmoides Oncorhynchus gorbuscha Pomacea canaliculata Rana huanrenesis Simocephalus vetulus Tubifex tubifex

37.6 267.8 885.9 311.2 143.9 684.7 162.6 106.3 53.4 95.5 281.5 106.9 170.2 218.7 89.06 99.15 82.3 172.2 142.9 216.5

This study This study This study This study US EPA (2013) This study US EPA (2013) US EPA (2013) This study This study US EPA (2013) US EPA (2013) US EPA (2013)) US EPA (2013) US EPA (2013)) US EPA (2013) This study This study US EPA (2013)) US EPA (2013)

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Fig. 3. Species sensitivity distribution curve of Korean freshwater aquatic organisms (genus) based on short-term LC50 values of total ammonia nitrogen (TAN).

provided by the technical guidance document (TGD) of European Union (EU) (ECB, 2003), PNEC, which is the same term as the acute water quality criteria in this study, is calculated using Eq. (3);

PNECð¼ Acute Water Quality CriteriaÞ ¼

HC5ðAcuteÞ AF

ð3Þ

where AF is an assessment factor between 1 and 5, contemplating the uncertainties of data (ECB, 2003). In this study, PNEC was calculated from HC5 divided by the assessment factor. An assessment factor of 2 was set to explain the uncertainty of missing taxonomic groups and provide a better protective margin.

2.6. Application of water quality criteria to nationwide monitoring data Currently, there are 905 water quality monitoring stations in operation in rivers and lakes throughout the nation: 336 stations in Han River, 254 stations in Nakdong River, 190 stations in Geum River, and 125 stations in Youngsan River (Fig. 1). We applied the water quality criteria derived in this study to the nationwide monitoring data in Korea to identify the number of data points that exceed the criteria. The data were acquired from the Water Information System managed by the National Institute of Environmental Research (http://water.nier.go.kr/ main/mainContent.do). We used the data measured from October 2016 to September 2017. These monitoring data were adjusted to TAN at pH 7 and 20 °C.

Fig. 4. Application of Korean criteria of total ammonia nitrogen (TAN) to the data monitored in four major rivers nationwide after the adjustment at pH 7 and 20 °C to identify the number of data points that exceed criteria.

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Table 5 The average and standard deviation of pH and temperature in four rivers.

Han River Nakdong River Geum River Youngsan River

Average of pH

Standard deviation of pH

Average of temperature

Standard deviation of temperature

7.9 7.9 7.8 7.6

0.6 0.5 0.5 0.4

15.4 16.3 15.7 15.9

8.8 8.0 8.2 8.0

3. Results and discussion 3.1. Fitness of the equation Since a geographical difference in species distribution may cause a deviation in toxicity values (Gao et al., 2014), water quality criteria should consider the characteristics of the regional environment (Wu et al., 2010). However, Maltby et al. (2005) proposed that while the species used to construct SSDs may affect the risk assessment, the geographical differences generally do not have a significant impact on the risk assessment. Feng et al. (2013) did not observe a significant difference between two distributions based on North American and nonNorth American species when they derived freshwater quality criteria for zinc. Because the findings of the prior studies were inconsistent about the toxicity of chemicals in different regions, it was necessary to verify the applicability of the equation of US EPA (2013) to Korea's aquatic ecosystems. When three Korean native aquatic species (A. chinensis, P. canaliculata, and D. galeata) were exposed to TAN at different pH, they showed a different toxicity response. The median lethal concentration increased with pH (Fig. 2, Table 2) because when pH increased, the concentration of NH3 increased and boosted the toxicity of unionized ammonia to organisms (Russo, 1985). Before pH and temperature were adjusted at pH 7 and 20 °C, the ratio of the maximum LC50 to minimum LC50 of TAN in A. chinensis, P. canaliculata, and D. galeata was 6.3, 6.0, and 2.8, respectively. After pH and temperature values were adjusted, the ratios decreased dramatically to 1.5, 1.2, and 1.3, respectively. When we used the equation that USEPA suggested to adjust LC50 to pH and temperature, the median lethal concentration of each species became closer to each other. This means that even though the values of LC50 of TAN vary with pH (Fig. 2, left), the variations in LC50 after its adjustment at pH 7 and 20 °C became narrower (Fig. 2, right). Therefore, the equation is applicable to Korean native aquatic species. 3.2. SSD curves and HC5 values The LC50 values for all tested organisms are presented in Table 3. Before pH and temperature values were adjusted, A. vernalis was the most

sensitive species among all the animal species tested with the lowest LC50 values, while C. kiiensis was the most insensitive species with the highest LC50 values. However, after pH and temperature were adjusted, there was a change in their sensitivity. The most sensitive species was the same, but the most insensitive species with the highest LC50 values changed from C. kiiensis to B. calyciflorus. In addition to nine Korean indigenous aquatic species, we used 11 species used in US EPA (2013). The results of LC50 in Table 4 were used to generate the species sensitivity distribution curves for Korean freshwater aquatic organisms. Based on the SSD curves, 95% protective concentrations (PC95) were calculated. The sample of toxicity data from a population that has a normal distribution can be assessed using goodness-of-fit tests (Vlaardingen et al., 2004). Goodness-of-fit test is to measure discrepancy between a statistical model and the data at hand. Using the data from Korean native aquatic species and from US EPA (2013), the normality tests of SSDs at the genus and species level were performed. Normality was accepted at the 5% critical value (Vlaardingen et al., 2004). Normality test was performed using software ETX 2.0. The result of the normality test for the “genus” of nine Korean native organisms and 11 organisms used in US EPA (2013) was proven “accepted” while that of the test with the “species” of nine Korean native organisms and 37 organisms used in US EPA (2013) was “rejected”. Based on the results of the goodness-of-fit test via EtX 2.0, we conclude that the sample of toxicity data with “genus” is normally distributed while the sample with species is not. In addition, the US EPA method uses genus mean toxicity values (GMTVs) instead of species mean toxicity values (SMTVs) to calculate HC5 to reduce the bias introduced by excessive species in some taxa (Wang et al., 2015). Based on the toxicity data in Tables 3 and 4, the SSD curve was constructed with a log-normal distribution and the simulated curve for freshwater is shown in Fig. 3. The positions of species at different parts of the SSD curve demonstrate the distribution patterns of the taxonomic groups that these species represent (Mensah et al., 2013). A. vernalis and D. galeata were the most sensitive taxa in the SSD curve (Fig. 3). In contrast, C. kiiensis and B. calyciflorus appeared at the right tail-end of the curve, showing their relative insensitivity to ammonia. At the center of the curve were Ceriodaphnia dubia, Chydorus sphaericus, Limnodrilus hoffmeisteri, and R. huanrenesis, suggesting that they are less sensitive to ammonia than midge and B. calyciflorus, but more sensitive than A. vernalis and D. galeata (Crustacean). This is confirmed in a previous study (Wang and Leung, 2015), in which midge was found to be less sensitive to ammonia than crustacean. Species sensitivity distribution curves can compare the toxicity of each species visually and provide the hazardous concentrations for 5% of the species (HC5), which are equivalent to the 95% protective concentration (PC95) (Hose, 2005). The HC5 values calculated in this study for TAN was 44 mg (TAN)/L after the adjustment at pH 7 and 20 °C. When we derived the criteria for TAN in the freshwater, the value of AF was set at 2 to explain the uncertainty of missing taxonomic groups and provide a better protective margin. 3.3. Application of water quality criteria to nationwide monitoring data

Fig. 5. Application of Korean criteria for total ammonia nitrogen (TAN) to the data monitored in lakes nationwide after the adjustment at pH 7 and 20 °C to identify the number of data points that exceeded the criteria.

We applied the ammonia criteria value derived in this study to the monitoring data of four major rivers to ascertain the percentage of sites that exceed the criteria. The data were acquired from the website http://water.nier.go.kr/main/mainContent.do. This website provides

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the monitoring data nationwide in Korean language. The data acquired from October 2016 to September 2017 were adjusted to pH 7 and 20 °C. After the adjustment, the data were compared to the criteria values. Fig. 4 shows the results of the comparisons between the monitored data and the criteria. Red squares represent the sites exceeding the criteria. The rate of exceeding the criteria in Han River, Nakdong River, Geum River, and Youngsan River is 0.51%, 0.09%, 0.18%, and 0.20%, respectively. When the data were compared before and after the adjustment of pH and temperature, the difference in ammonia concentrations varied significantly. At some sites, the ratio of the concentrations after the adjustment to those before the adjustment was 100. The ratios were 55, 54, 50, and 35 in Han River, Nakdong River, Geum River, and Youngsan River, which means that the adjusted TAN concentration is 35–55 times higher than the unadjusted concentration. Overall, when the temperature changes from 0 °C to 30 °C, the toxicity increases by 3.8 times. Meanwhile, when pH changes from 6.5 to 9.0, the toxicity rises dramatically by 37.1 times (US EPA, 2013). Owing to the high variations in the standard deviation of pH, the rate of excess in Han River was higher than that in other rivers (Table 5). As a result, taken into account local conditions in Korea, the limit of 22 mg/L (TAN) is acceptable, even though the rate of exceeding the criteria is low, because the criteria is the minimum concentration to protect 95% aquatic organisms. Furthermore, pH and temperature play an important role in determining TAN rather than the concentration itself and a source of TAN in monitoring sites. In the meantime, the rate of exceeding the criteria in lakes was 0.35%, higher than in Nakdong River, Geum River, and Youngsan River, but lower than in Han River (Fig. 5). Based on the data from four rivers and lakes nationwide, before the data were adjusted for pH and temperature, no data points exceeded the guideline. After the adjustment, however, the rate of exceeding the criteria increased significantly. This implies that the ammonia criteria have to be introduced because the unadjusted concentrations do not reflect the harmful effects of ammonia on aquatic organisms. 4. Conclusions This study was carried out to derive the criteria for ammonia in freshwater to protect aquatic life. Based on the species sensitivity distribution method using Korean indigenous aquatic biota, HC5 values calculated in this study were 44 mg TAN/L. The value of assessment factor was set at 2. Consequently, the criteria for ammonia were derived as 22 mg TAN/L at pH 7 and 20 °C. When this value was applied to the monitoring data nationwide, 0.51%, 0.09%, 0.18%, 0.20%, and 0.35% of monitoring sites in Han River, Nakdong River, Geum River, Youngsan River, and lakes nationwide, respectively, exceeded this criteria. The Ministry of Environment in Korea has been considering introducing water quality standard for protecting aquatic life. These results highlight the urgency and importance of establishing the standards for ammonia in Korea. Acknowledgement This work was supported by a grant from the National Institute of Environment Research (NIER), funded by the Ministry of Environment (MOE) of the Republic of Korea (NIER-2015-02-02-073). References ANZECC and ARMCANZ (Australian and New Zealand Environment and Conservation Council and Agriculture and Resources Management Council of Australia and New Zealand), 2000. National water quality management strategy paper no. 4. Australian and New Zealand Environment and Conservation Council and Agriculture and Resource Management Council of Australia and New Zealand, Canberra,

Australia. Australian and New Zealand Guidelines for Fresh and Marine Water Quality. 1, pp. 1–314. Brix, K.V., DeForest, D.K., Adams, W.J., 2001. Assessing acute and chronic copper risks to freshwater aquatic life using species sensitivity distributions for different taxonomic groups. Environm. Toxicol. Chem. 20, 1846–1856. Camargo, J., Alonso, A., 2006. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystem: a global assessment. Environ. Internat. 32, 831–849. CCME (Canadian Council of Ministers of the Environment), 2010. Canadian water quality guideline for the protection of aquatic life-ammonia. Canadian Environmental Quality Guidelines. Vol. 1999. Canadian Council of Ministers of the Environment, Winnipeg, Canada, pp. 1–8. Constable, M., Charlton, M., Jensen, F., McDonald, K., Craig, G., Taylor, K.W., 2003. An ecological risk assessment of ammonia in the aquatic environment. Hum. Eco. Risk Assess. 9 (2), 527–548. ECB (European Chemicals Bureau), 2003. Technical Guidance Document on Risk Assessment – Part. Vol. II. Institute of Health and Consumer Protection, Italy, Ispra. Emerson, K., Russo, R.C., Lund, R.E., Thurston, R.V., 1975. Aqueous ammonia equilibrium calculations; effect of pH and temperature. J. Fish. Res. Board Can. 32, 2378–2383. Environment Canada, 2001. Priority Substances Assessment Report: Ammonia in the Aquatic Environment. Minister of Public Works and Government Services Canada, Ottawa, On, Canada. Feng, C.L., Wu, F.C., Zhao, X.L., Chang, H., 2012. Water quality criteria research and progress. Sci. China. Earth Sci. 55 (6), 882–891. Feng, C.L., Wu, F.C., Dyer, S.D., Chang, H., Zhao, X.L., 2013. Derivation of freshwater quality criteria for zinc using interspecies correlation estimation models to protect aquatic life in China. Chemosphere 90, 1177–1183. Gao, P., Li, Z., Gibson, M., Gao, H., 2014. Ecological risk assessment of nonylphenol in coastal waters of China based on species sensitivity distribution model. Chemosphere 104, 113–119. Hose, G.C., 2005. Assessing the need for groundwater quality guidelines for pesticides using the species sensitivity distribution approach. Hum. Ecol. Risk. Assess. 11 (5), 951–966. Koojiman, S., 1987. A safety factor for LC50 values allowing for differences in sensitivity among species. Water Res. 21 (3), 269–276. Lang, T., Peters, G., Hoffmann, R., Meyer, E., 1987. Experimental investigations on the toxicity of ammonia: effects on ventilation frequency, growth, epidermal mucous cells, and gill structure of rainbow trout Salmo gairdneri. Dis. Aquat. Org. 3, 159–165. Maltby, L., Blake, N., Brock, T., Van Den Brink, P., 2005. Insecticide species sensitivity distribution: importance of test species selection and relevance to aquatic ecosystems. Environ. Toxicol. Chem. 24 (2), 379–388. Mensah, P.K., Palmer, C.G., Muller, W.J., 2013. Derivation of South African water quality guidelines for Roundup® using species sensitivity distribution. Ecotoxicol. Environ. Saf. 96, 24–31. Newman, M.C., Ownby, D.R., Mezin, L.C.A., Powell, D.C., Christensen, T.R.L., Lerberg, S.B., Anderson, B.A., 2000. Applying species-sensitivity distributions in ecological risk assessment: assumptions of distribution type and sufficient numbers of species. Environ. Toxicol. Chem. 19 (2), 508–515. Posthuma, L., Suter, G.W.I., Traas, T.P., 2002. Species Sensitivity Distributions in Ecotoxicology. Lews, Boca Raton, FL. Russo, R.C., 1985. Ammonia, nitrite and nitrate. In: Rand, G.M., Petrocelli, S.R. (Eds.), Fundamentals of Aquatic Toxicology. Hemisphere Publishing Corporation, Washington, D.C, pp. 455–471. US EPA, 2013. Aquatic Life Ambient Water Quality Criteria for Ammonia – Freshwater. pp. 5–6. Van Straalen, N.M., Denneman, C.A.J., 1989. Ecotoxicological evaluation of soil quality criteria. Ecotox. Environ. Safe. 18, 241–251. Van Wijngaarden, R.P.A., Arts, G.H.P., Belgers, J.D.M., Boonstra, H., Roessink, I., Schroer, A.F.W., Brock, T.C.M., 2010. The species sensitivity distribution approach compared to a microcosm study: a case study with the fungicide fluazinam. Ecotoxicol. Environ. Saf. 73, 109–122. Vlaardingen, P.L.A., Traas, T.P., Winstersen, A.M., Aldenberg, T., 2004. ETX2.0; A program to calculate hazardous concentrations and fraction affected, based on normally distributed toxicity data. RIVM Report 651501028. Wang, Z., Leung, K., 2015. Effects of unionized ammonia on tropical freshwater organisms: implications on temperate-to-tropic extrapolation and water quality guidelines. Environ. Pollut. 205, 240–249. Wang, X., Yan, X.Z., Liu, Z., Zhang, C., Wang, W., Li, H., 2014. Comparison of species sensitivity distributions for species from China and the USA. Environ. Sci. Pollut. Res. 21, 168–176. Wang, Y., Zhang, L., Meng, F., Zhou, Y., Jin, X., Giesy, J.P., Liu, F., 2015. Improvement on species sensitivity distribution methods for deriving site-specific water quality criteria. Environ. Sci. Pollut. Res. 22, 5271–5282. Wheeler, J.R., Grist, E.P.M., Leung, K.Y.M., Morritt, D., Crane, M., 2002. Species sensitivity distributions: data and model choice. Mar. Pollut. Bull. 45 (1–12), 192–202. Wintersen, A.M., Van Vlaardingen, P., Traas, T.P.T.A., 2004. In: NIfPHat, Environment (Ed.), A Program to Calculate Hazardous Concentrations and Fraction Affected, Based on Normally Distributed Toxicity Data. Bilthoven, The Netherlands. Wu, F., Meng, W., Zhao, X., Li, H., Zhang, R., Cao, Y., Liao, H., 2010. China embarking on development of its own national water quality criteria system. Environ Sci. Technol. 44, 7992–7993.