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The nonlinear relationship between nutrient ratios and salinity in estuarine ecosystems: implications for management
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The nonlinear relationship between nutrient ratios and salinity in estuarine ecosystems: implications for management Hon-Kit Lui and Chen-Tung Arthur Chen Riverine N and P fluxes have increased rapidly in recent decades, resulting in increased eutrophication of adjacent coasts. Since N fluxes have been rising faster than P fluxes, many rivers are P-limited. Therefore, upper estuaries are commonly P-limited whereas lower estuaries are frequently Nlimited, implying that nutrient management strategies should vary across an estuary. Since seawater contains relatively low nutrients, the water in an estuary with low salinity generally has a limiting nutrient the same as that of the riverine water. As the spatial distribution of eutrophicated regions and riverine plumes change temporally within estuaries and the adjacent coasts, the target of removal in sewage treatment is not necessarily the limiting nutrient of the river water. Sewage plant operators may use salinity to identify the approach of the riverine plume, and consider switching the plant from removing P to removing N, or vice versa, whenever a coastal area is or is likely to be threatened by hypoxia and harmful algal blooms. Address Institute of Marine Geology and Chemistry, National Sun Yat-sen University, 80424 Kaohsiung, Taiwan Corresponding author: Chen, Chen-Tung Arthur ([email protected])
Current Opinion in Environmental Sustainability 2012, 4:227–232 This review comes from a themed issue on Carbon and nitrogen cycles Edited by Chen-Tung Arthur Chen and Dennis Peter Swaney Received 14 February 2012; Accepted 17 March 2012 Available online 7th April 2012 1877-3435/$ – see front matter # 2012 Elsevier B.V. All rights reserved. DOI 10.1016/j.cosust.2012.03.002
Introduction Rivers bring terrestrial materials, such as organic matter and nutrients, through estuaries to oceans, supporting an important part of new/export production in the oceans [1]. In recent decades, riverine N and P fluxes have increased several folds over their original values, causing eutrophication of adjacent coasts [2–4]. Consequently, hypoxia has spread widely [5–7] and harmful algal blooms (HABs) now occur frequently [8–10], as demonstrated by such incidents as the recently reported jellyfish blooms in the East China Sea and Sea of Japan [11–13]. In 1970, 60 ecosystems were reportedly under hypoxia; that number www.sciencedirect.com
reached 300 in 1990 and over 400 in 2007, when they covered more than 245 000 km2 of the sea bottom [5]. Observations reveal that in some cases, the complexities of hydrology and biogeochemical processes prevent estuarine ecosystems from returning to their original condition after hypoxia, even when nutrient loadings are reduced to their initial values [14,15,16–18,19]. This finding suggests that a greater effort must be made for the recovery of an estuary from hypoxia than to prevent hypoxia in the first place. Therefore, knowledge of the nutrient that limits the growth of phytoplankton is critical in developing effective nutrient management practices to ensure the sustainable development of coastal zones. In aquatic ecosystems, the limiting nutrient is the nutrient that is insufficient to support the primary productivity. Mainly owing to mixing with N-limited seawater and partly owing to high denitrification rate in estuaries [20], N generally appears to be the limiting nutrient in lower estuaries, in high-salinity regions, or whenever the river discharge is low. In the upper estuaries, the pattern is not so clear. The extensive use of N fertilizers in agriculture [21–23] explains why riverine N fluxes rises more rapidly than does P flux, resulting in high dissolved inorganic nitrogen (DIN) to soluble reactive phosphate (SRP) ratios in many rivers, including the Yangtze, Mississippi, and Pearl rivers. N has been suggested to be more likely to induce hypoxia in the Gulf of Mexico [3,24–26], while the Pearl River estuary has been suggested to be P-limited [27–30]. However, insufficient data and indirect evidence leave the matter of whether N or P is the limiting nutrient in estuarine ecosystems contentious [3,24,31].
Management strategy and salinity application For freshwater and seawater end-members with the same limiting nutrient, simply reducing the amount of limiting nutrient helps to reduce the degree of eutrophication. However, the situation is more complex when freshwater and seawater have different limiting nutrients. The most common case involves the mixing of P-limited riverine water with N-limited seawater. In estuaries that are influenced by P-limited riverine water, the low-salinity regions are normally P-limited, while the high-salinity regions, as well as the adjacent coasts, are commonly N-limited [30,32–36]. Previous studies have suggested that a shift in the limiting nutrient in an estuary is a salinity-related phenomenon [36–38]. Based on a simple mixing model, Lui and Current Opinion in Environmental Sustainability 2012, 4:227–232
228 Carbon and nitrogen cycles
Chen (2011) [39] recently demonstrated that the nutrient ratio is a nonlinear function of salinity. When a particular salinity is reached, the estuary shifts from one limiting nutrient to another if the freshwater and seawater end-members have different limiting nutrients. Interestingly, the salinity at which the limiting nutrient changes is a function of the biological consumption ratio in nutrients. However, such a shift can also be related to other processes, such as the supply of additional P from sewage input [32], sediment release [40], or the removal of N by denitrification [20,33]. Therefore, salinity at which the limiting nutrient shifts differ from estuary to estuary. Since seawater contains relatively low nutrients, the water in an estuary with low salinity generally has a limiting status the same as that of the riverine water. That is, sewage plant operators may use salinity as one of the parameters to decide when the riverine plume has reached the eutrophicated regions within or off estuaries, and when to switch the plant to reduce N or P. Since the spatial distribution of eutrophicated regions and riverine plumes change temporally within and off estuaries, whether N or P inputs must be managed to reduce the degree of eutrophication in estuarine ecosystems depends on the particular situation. Here four conceptual frameworks for nutrient management strategies are presented, and the mixing of P-limited riverine water with N-limited seawater, and vice versa, are considered as examples (Figure 1).
Figure 1 shows four cases of eutrophication. Case one refers to a well-mixed estuary that is not, and is not likely to be, eutrophicated. In this case, no specific nutrient has to be reduced if the incoming nutrient loadings do not threaten the estuary. A notable example is the Delaware Estuary, where despite high nutrient loadings and primary production, no obvious sign of eutrophication or hypoxia is present, owing to the thorough mixing [41,42]. Case two refers to an estuary in which the P-limited upper estuary, but not the N-limited lower estuary, is or tends to be eutrophicated (Figure 1). In this case, the flux of P needs to be reduced when hypoxia occurs in the P-limited water column. This situation resembles that in the Pearl River Estuary, where Hong Kong, which has over 7 million inhabitants, is located. The use of salinity in sewage management is illustrated herein with reference to the Pearl River Estuary as an example. Figure 2 shows time series of salinity, chlorophyll-a, and the saturation state of dissolved oxygen (DO%) at a station south of Hong Kong. In summer, the nutrient-enriched Pearl River water enters the study site and enhances local primary production, resulting in low salinity but a high concentration of chlorophyll-a and DO% in the surface water. During that season, the bottom water with high salinity but low chlorophyll-a concentration has a low DO%, possibly because of the combination of summer stratification and decomposition of organic matter from
Figure 1
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Conceptual frameworks for nutrient management in estuary where P-limited riverine water mixes with N-limited seawater. Dashed lines represent salinity at which P limitation shifts to N limitation. In case 1, no hypoxia is present and no nutrient removal is necessary. In case 2, hypoxia is present in the P-limited region and P must be removed. In case 3, hypoxia is present in the N-limited region and N must be removed. In case 4, hypoxia is present in both P-limited and N-limited regions and both nutrients must be removed. Current Opinion in Environmental Sustainability 2012, 4:227–232
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Relationship between nutrient ratios and salinity Lui and Chen 229
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usually occur in the salinity range in which the water column is limited by P. P is generally depleted during algal blooms [39]. As illustrated above, phosphate should be the primary concern in reducing the eutrophication, hypoxia and frequency of HABs during summer [29,45]. Briefly, phosphate rather than nitrogen should be the target of the Hong Kong SMPs. Case 3 refers to an estuary in which the N-limited lower estuary, but not the P-limited upper estuary, is or tends to be eutrophicated (Figure 1). In this case, the flux of N needs to be reduced. This situation resembles that in the Mississippi River. The riverine N loading is a more accurate indicator than P loading in predicting the area of hypoxia in the Gulf of Mexico [25,46]. As the Mississippi River discharges directly into the Gulf of Mexico, the freshwater plume changes rapidly from P to N-limited as the river water mixes with a massive amount of Nlimited seawater. Therefore, inorganic nitrogen that originates from both riverine water and seawater governs the production of phytoplankton off the mouth of the Mississippi River.
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Time series of salinity, concentration of chlorophyll-a (Chl-a), and saturation state of dissolved oxygen (DO) in surface and bottom waters at station SM18, south of Hong Kong. (See Lui and Chen (2011) [39] for sampling location.) Sampling depths of surface and bottom waters were 1 m below water surface and 1 m above the seabed, respectively. Data are provided by the Hong Kong Environmental Protection Department.
the surface water. In winter, the water of the Pearl River barely enters the study area, and both surface and bottom water have equally high salinity and DO% but are low in chlorophyll-a concentration (Figure 2). This situation is analogous to case 1 when the amount of no specific nutrient needs to be reduced. Therefore, the sewage treatment plant may have not to reduce any nutrients in winter, but it must remove P from the submarine sewage outfall in summer when salinities reach a low threshold [43]. This example shows that sewage treatment plant operators can take advantage of ease of monitoring salinity to decide when to operate, and when to remove which nutrient. The Hong Kong government has implemented Sewerage Master Plans (SMPs) to improve the quality of coastal water. Stage one of the plan (Harbor Area Treatment Scheme) began in late 2001, and stage two (i.e. expanding the current Stonecutters Island Sewage Treatment Works) is scheduled to be completed by 2013–14. With respect to the control of nutrients, SMPs are developed to promote a situation in which the concentration of inorganic nitrogen should not exceed 0.3 mg/l at Mirs Bay, or 0.7 mg/l at Deep Bay [43,44]. However, Hong Kong coastal water contains nutrients from the Pearl River as well as local sewage discharge. Furthermore, algal blooms www.sciencedirect.com
Case 4 refers to an estuary in which both the P-limited upper estuary and N-limited lower estuary are or tend to be eutrophicated (Figure 1). In this case, fluxes of both N and P need to be reduced. Reducing P alone reduces the production and, subsequently, the degree of eutrophication at places only where P is limiting. However, the excess riverine N still combines with excess P in incoming seawater to meet the biological demand at the Nlimited lower estuary. Although reducing the flux of N may help to reduce the degree of hypoxia at the lower estuary, it may not have a positive effect in the upper estuary unless it is also reduced to such an extent that the upper estuary is changed from P to N-limited. Reducing the flux of a single nutrient is thus unlikely to reduce the degree of hypoxia throughout the system. For instance, in the Neuse River estuary [47,48], an increased supply of P raises the biological consumption of riverine N in the upper estuary, subsequently reducing N there. A reduction in P loading through wastewater treatment in the upper estuary increases the amount of riverine N that reaches the lower estuary. Consequently, eutrophication occurs when the river water encounters the seawater, which happens to be N-limited.
Changing nutrient inventories As salinity is the deciding parameter, we then use it to evaluate the changing nutrient inventories and to illustrate the shift from P to N limitation, as well as certain implications in nutrient management in the Pearl River Estuary. N-limited seawater in the northern South China Sea has DIN and SRP concentrations of 3.01 mmol kg 1 and 0.30 mmol kg 1, respectively. The corresponding values for P-limited Pearl River water are 140 mmol kg 1 and 2.25 mmol kg 1, respectively [39]. Accordingly, the Pearl Current Opinion in Environmental Sustainability 2012, 4:227–232
230 Carbon and nitrogen cycles
Figure 3 30 Seawater River water
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Mass of seawater mixed with one kg of the Pearl River water Current Opinion in Environmental Sustainability
Categories of biological productions that are supported by mixing 1 kg of Pearl River water with 40, 58, and 80 kg of seawater. DIN and SRP inventories are plotted on a scale of 1:16. Category I is supported by river water. Category II is supported by both river and seawater. Category III is supported by seawater.
inventory and 89% of the total SRP inventory to balance the excess riverine DIN. Mixing with more seawater makes the water in the estuary N-limited. Although reducing the amount of P may reduce the degree of hypoxia by limiting the biological production in the upper estuary, it may worsen in the lower estuary where more riverine N is encountered. This fact may help to explain why in some cases riverine N but not P loadings cause eutrophication in estuaries that are influenced by P-limited riverine waters [3,24–26,49–51].
Conclusions The nonlinear response of estuarine ecosystems to changes in nutrient loadings suggests the importance of preventing hypoxia in estuarine ecosystems rather than treating them after hypoxia has already occurred. A flexible management scheme that is based on hydrological variability is proposed herein to show that the target of nutrient removal is not necessarily the limiting nutrient of the river water. This management scheme will hopefully provide technologically and economically feasible easy guidelines for sewage plant operators concerning when they should switch the plant from removing P to removing N, or vice versa.
Acknowledgements River water contains (140 2.25 16) = 104 mmol of DIN in excess of the amount required to consume all SRP. On the contrary, 1 kg of seawater can provide (0.30 3.01/16) = 0.112 mmol of excess SRP. Therefore, 104/(0.112 16) = 58.0 kg of seawater can balance the excess DIN in 1 kg of the Pearl River water. Also, the N and P inventories of 1 kg Pearl River mixed with 40 kg, 58 kg, and 80 kg of its ambient seawater are used to illustrate the biological production that is supported by the riverine water and seawater inputs (Figure 3). Notably, estuarine waters with the above mentioned three mixed ratios have a salinity of >33, showing that estuarine water with low salinity generally has a limiting status the same as that of the riverine water. A shift from P to N limitation by mixing P-limited riverine water and N-limited seawater usually happens in high salinity regions, such as in the lower estuaries, or in the adjacent coasts. That is, the salinity in general can be used to identify the approaching riverine plume and the target of nutrient removal, particularly, in a physical mixing dominated estuary. Production that is supported by the P-limited riverine water and N-limited seawater can be divided into three categories. The production of category (I), which is limited by riverine SRP, is supported by riverine input. The production of category (II) is supported by the combination of excess riverine DIN and excess seawater SRP. The production of category (III), which is limited by seawater DIN, is supported by seawater. In the above example, when 1 kg of riverine water is mixed with 58 kg of seawater, seawater contributes 55% of the total DIN Current Opinion in Environmental Sustainability 2012, 4:227–232
The authors would like to thank the Hong Kong Environmental Protection Department for providing invaluable data, and the Aim for the Top University Program and the National Science Council NSC 98-2621-M-110001-MY3 and 99-2611-M-110-002-MY3, Taiwan, for financially supporting this research. Dennis Swaney and three anonymous reviewers provided valuable comments that strengthened the manuscript.
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The nonlinear relationship between nutrient ratios and salinity in estuarine ecosystems: implications for management Hon-Kit Lui and Chen-Tung Arthur Chen Riverine N and P fluxes have increased rapidly in recent decades, resulting in increased eutrophication of adjacent coasts. Since N fluxes have been rising faster than P fluxes, many rivers are P-limited. Therefore, upper estuaries are commonly P-limited whereas lower estuaries are frequently Nlimited, implying that nutrient management strategies should vary across an estuary. Since seawater contains relatively low nutrients, the water in an estuary with low salinity generally has a limiting nutrient the same as that of the riverine water. As the spatial distribution of eutrophicated regions and riverine plumes change temporally within estuaries and the adjacent coasts, the target of removal in sewage treatment is not necessarily the limiting nutrient of the river water. Sewage plant operators may use salinity to identify the approach of the riverine plume, and consider switching the plant from removing P to removing N, or vice versa, whenever a coastal area is or is likely to be threatened by hypoxia and harmful algal blooms. Address Institute of Marine Geology and Chemistry, National Sun Yat-sen University, 80424 Kaohsiung, Taiwan Corresponding author: Chen, Chen-Tung Arthur ([email protected])
Current Opinion in Environmental Sustainability 2012, 4:227–232 This review comes from a themed issue on Carbon and nitrogen cycles Edited by Chen-Tung Arthur Chen and Dennis Peter Swaney Received 14 February 2012; Accepted 17 March 2012 Available online 7th April 2012 1877-3435/$ – see front matter # 2012 Elsevier B.V. All rights reserved. DOI 10.1016/j.cosust.2012.03.002
Introduction Rivers bring terrestrial materials, such as organic matter and nutrients, through estuaries to oceans, supporting an important part of new/export production in the oceans [1]. In recent decades, riverine N and P fluxes have increased several folds over their original values, causing eutrophication of adjacent coasts [2–4]. Consequently, hypoxia has spread widely [5–7] and harmful algal blooms (HABs) now occur frequently [8–10], as demonstrated by such incidents as the recently reported jellyfish blooms in the East China Sea and Sea of Japan [11–13]. In 1970, 60 ecosystems were reportedly under hypoxia; that number www.sciencedirect.com
reached 300 in 1990 and over 400 in 2007, when they covered more than 245 000 km2 of the sea bottom [5]. Observations reveal that in some cases, the complexities of hydrology and biogeochemical processes prevent estuarine ecosystems from returning to their original condition after hypoxia, even when nutrient loadings are reduced to their initial values [14,15,16–18,19]. This finding suggests that a greater effort must be made for the recovery of an estuary from hypoxia than to prevent hypoxia in the first place. Therefore, knowledge of the nutrient that limits the growth of phytoplankton is critical in developing effective nutrient management practices to ensure the sustainable development of coastal zones. In aquatic ecosystems, the limiting nutrient is the nutrient that is insufficient to support the primary productivity. Mainly owing to mixing with N-limited seawater and partly owing to high denitrification rate in estuaries [20], N generally appears to be the limiting nutrient in lower estuaries, in high-salinity regions, or whenever the river discharge is low. In the upper estuaries, the pattern is not so clear. The extensive use of N fertilizers in agriculture [21–23] explains why riverine N fluxes rises more rapidly than does P flux, resulting in high dissolved inorganic nitrogen (DIN) to soluble reactive phosphate (SRP) ratios in many rivers, including the Yangtze, Mississippi, and Pearl rivers. N has been suggested to be more likely to induce hypoxia in the Gulf of Mexico [3,24–26], while the Pearl River estuary has been suggested to be P-limited [27–30]. However, insufficient data and indirect evidence leave the matter of whether N or P is the limiting nutrient in estuarine ecosystems contentious [3,24,31].
Management strategy and salinity application For freshwater and seawater end-members with the same limiting nutrient, simply reducing the amount of limiting nutrient helps to reduce the degree of eutrophication. However, the situation is more complex when freshwater and seawater have different limiting nutrients. The most common case involves the mixing of P-limited riverine water with N-limited seawater. In estuaries that are influenced by P-limited riverine water, the low-salinity regions are normally P-limited, while the high-salinity regions, as well as the adjacent coasts, are commonly N-limited [30,32–36]. Previous studies have suggested that a shift in the limiting nutrient in an estuary is a salinity-related phenomenon [36–38]. Based on a simple mixing model, Lui and Current Opinion in Environmental Sustainability 2012, 4:227–232
228 Carbon and nitrogen cycles
Chen (2011) [39] recently demonstrated that the nutrient ratio is a nonlinear function of salinity. When a particular salinity is reached, the estuary shifts from one limiting nutrient to another if the freshwater and seawater end-members have different limiting nutrients. Interestingly, the salinity at which the limiting nutrient changes is a function of the biological consumption ratio in nutrients. However, such a shift can also be related to other processes, such as the supply of additional P from sewage input [32], sediment release [40], or the removal of N by denitrification [20,33]. Therefore, salinity at which the limiting nutrient shifts differ from estuary to estuary. Since seawater contains relatively low nutrients, the water in an estuary with low salinity generally has a limiting status the same as that of the riverine water. That is, sewage plant operators may use salinity as one of the parameters to decide when the riverine plume has reached the eutrophicated regions within or off estuaries, and when to switch the plant to reduce N or P. Since the spatial distribution of eutrophicated regions and riverine plumes change temporally within and off estuaries, whether N or P inputs must be managed to reduce the degree of eutrophication in estuarine ecosystems depends on the particular situation. Here four conceptual frameworks for nutrient management strategies are presented, and the mixing of P-limited riverine water with N-limited seawater, and vice versa, are considered as examples (Figure 1).
Figure 1 shows four cases of eutrophication. Case one refers to a well-mixed estuary that is not, and is not likely to be, eutrophicated. In this case, no specific nutrient has to be reduced if the incoming nutrient loadings do not threaten the estuary. A notable example is the Delaware Estuary, where despite high nutrient loadings and primary production, no obvious sign of eutrophication or hypoxia is present, owing to the thorough mixing [41,42]. Case two refers to an estuary in which the P-limited upper estuary, but not the N-limited lower estuary, is or tends to be eutrophicated (Figure 1). In this case, the flux of P needs to be reduced when hypoxia occurs in the P-limited water column. This situation resembles that in the Pearl River Estuary, where Hong Kong, which has over 7 million inhabitants, is located. The use of salinity in sewage management is illustrated herein with reference to the Pearl River Estuary as an example. Figure 2 shows time series of salinity, chlorophyll-a, and the saturation state of dissolved oxygen (DO%) at a station south of Hong Kong. In summer, the nutrient-enriched Pearl River water enters the study site and enhances local primary production, resulting in low salinity but a high concentration of chlorophyll-a and DO% in the surface water. During that season, the bottom water with high salinity but low chlorophyll-a concentration has a low DO%, possibly because of the combination of summer stratification and decomposition of organic matter from
Figure 1
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Case 2 N Limitation
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Conceptual frameworks for nutrient management in estuary where P-limited riverine water mixes with N-limited seawater. Dashed lines represent salinity at which P limitation shifts to N limitation. In case 1, no hypoxia is present and no nutrient removal is necessary. In case 2, hypoxia is present in the P-limited region and P must be removed. In case 3, hypoxia is present in the N-limited region and N must be removed. In case 4, hypoxia is present in both P-limited and N-limited regions and both nutrients must be removed. Current Opinion in Environmental Sustainability 2012, 4:227–232
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Relationship between nutrient ratios and salinity Lui and Chen 229
DO (%)
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usually occur in the salinity range in which the water column is limited by P. P is generally depleted during algal blooms [39]. As illustrated above, phosphate should be the primary concern in reducing the eutrophication, hypoxia and frequency of HABs during summer [29,45]. Briefly, phosphate rather than nitrogen should be the target of the Hong Kong SMPs. Case 3 refers to an estuary in which the N-limited lower estuary, but not the P-limited upper estuary, is or tends to be eutrophicated (Figure 1). In this case, the flux of N needs to be reduced. This situation resembles that in the Mississippi River. The riverine N loading is a more accurate indicator than P loading in predicting the area of hypoxia in the Gulf of Mexico [25,46]. As the Mississippi River discharges directly into the Gulf of Mexico, the freshwater plume changes rapidly from P to N-limited as the river water mixes with a massive amount of Nlimited seawater. Therefore, inorganic nitrogen that originates from both riverine water and seawater governs the production of phytoplankton off the mouth of the Mississippi River.
Current Opinion in Environmental Sustainability
Time series of salinity, concentration of chlorophyll-a (Chl-a), and saturation state of dissolved oxygen (DO) in surface and bottom waters at station SM18, south of Hong Kong. (See Lui and Chen (2011) [39] for sampling location.) Sampling depths of surface and bottom waters were 1 m below water surface and 1 m above the seabed, respectively. Data are provided by the Hong Kong Environmental Protection Department.
the surface water. In winter, the water of the Pearl River barely enters the study area, and both surface and bottom water have equally high salinity and DO% but are low in chlorophyll-a concentration (Figure 2). This situation is analogous to case 1 when the amount of no specific nutrient needs to be reduced. Therefore, the sewage treatment plant may have not to reduce any nutrients in winter, but it must remove P from the submarine sewage outfall in summer when salinities reach a low threshold [43]. This example shows that sewage treatment plant operators can take advantage of ease of monitoring salinity to decide when to operate, and when to remove which nutrient. The Hong Kong government has implemented Sewerage Master Plans (SMPs) to improve the quality of coastal water. Stage one of the plan (Harbor Area Treatment Scheme) began in late 2001, and stage two (i.e. expanding the current Stonecutters Island Sewage Treatment Works) is scheduled to be completed by 2013–14. With respect to the control of nutrients, SMPs are developed to promote a situation in which the concentration of inorganic nitrogen should not exceed 0.3 mg/l at Mirs Bay, or 0.7 mg/l at Deep Bay [43,44]. However, Hong Kong coastal water contains nutrients from the Pearl River as well as local sewage discharge. Furthermore, algal blooms www.sciencedirect.com
Case 4 refers to an estuary in which both the P-limited upper estuary and N-limited lower estuary are or tend to be eutrophicated (Figure 1). In this case, fluxes of both N and P need to be reduced. Reducing P alone reduces the production and, subsequently, the degree of eutrophication at places only where P is limiting. However, the excess riverine N still combines with excess P in incoming seawater to meet the biological demand at the Nlimited lower estuary. Although reducing the flux of N may help to reduce the degree of hypoxia at the lower estuary, it may not have a positive effect in the upper estuary unless it is also reduced to such an extent that the upper estuary is changed from P to N-limited. Reducing the flux of a single nutrient is thus unlikely to reduce the degree of hypoxia throughout the system. For instance, in the Neuse River estuary [47,48], an increased supply of P raises the biological consumption of riverine N in the upper estuary, subsequently reducing N there. A reduction in P loading through wastewater treatment in the upper estuary increases the amount of riverine N that reaches the lower estuary. Consequently, eutrophication occurs when the river water encounters the seawater, which happens to be N-limited.
Changing nutrient inventories As salinity is the deciding parameter, we then use it to evaluate the changing nutrient inventories and to illustrate the shift from P to N limitation, as well as certain implications in nutrient management in the Pearl River Estuary. N-limited seawater in the northern South China Sea has DIN and SRP concentrations of 3.01 mmol kg 1 and 0.30 mmol kg 1, respectively. The corresponding values for P-limited Pearl River water are 140 mmol kg 1 and 2.25 mmol kg 1, respectively [39]. Accordingly, the Pearl Current Opinion in Environmental Sustainability 2012, 4:227–232
230 Carbon and nitrogen cycles
Figure 3 30 Seawater River water
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Mass of seawater mixed with one kg of the Pearl River water Current Opinion in Environmental Sustainability
Categories of biological productions that are supported by mixing 1 kg of Pearl River water with 40, 58, and 80 kg of seawater. DIN and SRP inventories are plotted on a scale of 1:16. Category I is supported by river water. Category II is supported by both river and seawater. Category III is supported by seawater.
inventory and 89% of the total SRP inventory to balance the excess riverine DIN. Mixing with more seawater makes the water in the estuary N-limited. Although reducing the amount of P may reduce the degree of hypoxia by limiting the biological production in the upper estuary, it may worsen in the lower estuary where more riverine N is encountered. This fact may help to explain why in some cases riverine N but not P loadings cause eutrophication in estuaries that are influenced by P-limited riverine waters [3,24–26,49–51].
Conclusions The nonlinear response of estuarine ecosystems to changes in nutrient loadings suggests the importance of preventing hypoxia in estuarine ecosystems rather than treating them after hypoxia has already occurred. A flexible management scheme that is based on hydrological variability is proposed herein to show that the target of nutrient removal is not necessarily the limiting nutrient of the river water. This management scheme will hopefully provide technologically and economically feasible easy guidelines for sewage plant operators concerning when they should switch the plant from removing P to removing N, or vice versa.
Acknowledgements River water contains (140 2.25 16) = 104 mmol of DIN in excess of the amount required to consume all SRP. On the contrary, 1 kg of seawater can provide (0.30 3.01/16) = 0.112 mmol of excess SRP. Therefore, 104/(0.112 16) = 58.0 kg of seawater can balance the excess DIN in 1 kg of the Pearl River water. Also, the N and P inventories of 1 kg Pearl River mixed with 40 kg, 58 kg, and 80 kg of its ambient seawater are used to illustrate the biological production that is supported by the riverine water and seawater inputs (Figure 3). Notably, estuarine waters with the above mentioned three mixed ratios have a salinity of >33, showing that estuarine water with low salinity generally has a limiting status the same as that of the riverine water. A shift from P to N limitation by mixing P-limited riverine water and N-limited seawater usually happens in high salinity regions, such as in the lower estuaries, or in the adjacent coasts. That is, the salinity in general can be used to identify the approaching riverine plume and the target of nutrient removal, particularly, in a physical mixing dominated estuary. Production that is supported by the P-limited riverine water and N-limited seawater can be divided into three categories. The production of category (I), which is limited by riverine SRP, is supported by riverine input. The production of category (II) is supported by the combination of excess riverine DIN and excess seawater SRP. The production of category (III), which is limited by seawater DIN, is supported by seawater. In the above example, when 1 kg of riverine water is mixed with 58 kg of seawater, seawater contributes 55% of the total DIN Current Opinion in Environmental Sustainability 2012, 4:227–232
The authors would like to thank the Hong Kong Environmental Protection Department for providing invaluable data, and the Aim for the Top University Program and the National Science Council NSC 98-2621-M-110001-MY3 and 99-2611-M-110-002-MY3, Taiwan, for financially supporting this research. Dennis Swaney and three anonymous reviewers provided valuable comments that strengthened the manuscript.
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