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Relative importance of external and internal phosphorus loadings on affecting lake water quality in agricultural landscapes
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Relative importance of external and internal phosphorus loadings on affecting lake water quality in agricultural landscapes Keunyea Song a,∗ , Craig J. Adams b , Amy J. Burgin a a b
University of Kansas and Kanas Biological Survey, University of Kansas, 2101 Constant Ave., Lawrence, KS, 66047 USA School of Natural Resources, University of Nebraska-Lincoln, 3310 Holdrege Street, Lincoln, NE, 68583 USA
a r t i c l e
i n f o
Article history: Received 31 March 2017 Received in revised form 5 June 2017 Accepted 5 June 2017 Available online xxx Keywords: Agricultural reservoir Eutrophication External P loading Internal P loading Flow-through sediment core incubation
a b s t r a c t Internal phosphorus (P) loading from the sediment poses a high risk of being an additional P source to deteriorate water quality. Previous studies hypothesized that internal P loads can be as high as external P inputs, especially in P enriched landscapes such as agricultural areas. However, internal P loadings in eutrophic conditions are rarely quantified or compared with external P loads. In this study, we aimed to answer these three questions; 1) how much P is internally released from the sediment of hypereutrophic lakes? 2) how much do internal P loads contribute to lake water quality compared to external loads? and 3) what factors regulate the release and retention of P in the sediment? We selected four hypereutrophic lakes located in Eastern Nebraska. In the study lakes and watersheds, internal and external P loads were quantified in 2014. Total P concentrations of inflow water collected from primary water channels feeding the study lakes and daily inflow water discharge rates were used to calculate external P loads. Internal P loads were quantified from flow-through soil core incubation experiments. External TP loads varied temporarily depending on the changes in discharge, and were highest during spring storm events. The majority of internal P loading (i.e. P release from sediment) occurred in the summer when lakes experience strong stratification (i.e. anaerobic conditions). This is likely associated with oxygen availability in the sediments and chemical dissolution of P. By comparing the annual-scale of external and internal P inputs, external P loadings were still the dominant P source to the lakes, contributing up to 98% of the total P input whereas internal P loadings accounted for 4–12% of the total P input. Although internal P loads were relatively minor on an annual time scale, we found that summer internal loadings in some of study lakes exceeded their external loadings. Our results confirmed the dominant influence of external P loadings on water quality in the reservoirs. This suggests that non-point source controls and watershed management strategies to reduce external loadings should be implemented prior to internal P loading controls. Internal P loadings can be a significant P source, even if just temporarily, worsening water quality of agricultural reservoirs and downstream ecosystems in the summer. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Eutrophication is one of the most common water quality problems in the world. Nearly half of all US lakes are impaired by eutrophication, mainly from excessive phosphorus (P) loading (Carpenter et al., 1999; Dodds et al., 2009; Smith and Schindler, 2009). Eutrophication results in harmful algal blooms, hypoxia in coastal areas and loss of biodiversity. Such water quality deterioration is estimated to cause an annual loss of approximately $ 2.2 billion in the US (Dodds et al., 2009).
∗ Corresponding author. E-mail address: [email protected] (K. Song).
Agricultural activity is one of the major contributors of P to aquatic ecosystems (Kleinman et al., 2011; Royer et al., 2006; Schippers et al., 2006). The use of P in agricultural fertilizer has increased 3.5 times since 1960 and is expected to continue increasing (Smil, 2000; Tilman et al., 2001). Phosphorus is a necessary nutrient for crop production, and also the limiting nutrient for primary productivity in freshwater (Elser et al., 2007; Smil, 2000; Smith and Schindler, 2009). Phosphorus carried with water through rivers and stream channels in watersheds to downstream, lakes or reservoirs, is called external P loading. Variation in external P loading to lakes is driven by the timing of fertilizer application, crop production, soil type, and rainfall patterns (Royer et al., 2006). Once P enters into lakes, it can go through an internal cycle within foodwebs or be retained in the sediment, which accumulates over time, creating P and organic matter enriched sediment (Das et al., 2012;
http://dx.doi.org/10.1016/j.ecoleng.2017.06.008 0925-8574/© 2017 Elsevier B.V. All rights reserved.
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Søndergaard et al., 1993). Inorganic P can be chemically bound and deposited in sediments. Sediments also contain high loads of organic or particulate P, which can be released from decomposition (Song and Burgin, 2017). Sediment P concentrations can be 100X higher than water column concentrations, especially when excessive external P loads persist over time, such as in agricultural watersheds (Diaz et al., 2006; Reddy et al., 1999). Phosphorus enriched sediment is problematic because sediment P can be released back into the water column, a phenomenon termed internal loading. Lack of oxygen, pH changes, or decomposition can trigger internal P loading (Hupfer and Lewandowski, 2008; Jensen and Andersen, 1992; Pettersson, 1998). For example, in summer when strong stratification prevents the vertical exchange of materials in lakes and creates hypoxia in the sediment, chemically bound P is released (Nürnberg, 1987; Pettersson, 1998). Decomposition, mainly under aerobic conditions breaks down organic matter and releases inorganic or dissolved organic P into water columns (Hupfer and Lewandowski, 2008; Song and Burgin, 2017). As lakes eutrophy, internal P loading becomes a potentially large P source compared to external P loading (Coveney et al., 2005; Hamilton, 2012). Despite the potential for internal P loading to deteriorate water quality, especially in eutrophic or hypereutrophic lakes, internal P loading is rarely quantified and directly compared to external P loading. Therefore, we asked: 1) How much P is internally released from the sediment of hypereutrophic lakes? 2) How much do internal P loads contribute to lake water quality compared to external loads? and 3) What factors regulate the release and retention of P in the sediment? To answer these questions, we quantified both internal and external P loads in four hypereutrophic lakes within agricultural landscapes. Flow-through sediment core incubation experiments under anaerobic and aerobic conditions to quantify internal P loadings. 2. Materials and methods 2.1. Site description We selected four lakes located in Eastern Nebraska for this study. The study lakes (Table 1) were constructed in the 1960s primarily for water storage and have been restored through sediment dredging and watershed management in the last 20 years. All study reservoirs have similar morphological characteristics-surface area, water depth, and surrounding landscapes (Table 1). Agricultural areas make up 50–75% of their watersheds. All of them are considered to be in eutrophic-hypereutrophic states, as indicated by chlorophyll-a contents and total phosphorus (TP) concentrations in summer (Song and Burgin, 2017). 2.1.1. Lake water quality monitoring Water samples were collected biweekly at the deepest locations from the epilimnion using a Van Dorn sampler. A Garmin Legend CX-GPS was used for positioning to ensure samples were consistently collected from the same locations. Water sampling was conducted from June to Nov. 2014. Collected water samples were acidified immediately in the field. The samples were then digested in the laboratory using potassium persulfate and analyzed via a Flow Injection Analyzer (Astoria Pacific A2) for TP concentrations using the molybdate blue colorimetric method (USEPA 1993, Method 365.1). 2.1.2. Quantification of external P loadings Inflow water samples from primary water channels feeding the study lakes were collected through baseflow water sampling and stormwater sampling. Baseflow water samples (flow during
dry weather conditions) were gathered biweekly by grab sampling. Storm water samples (flow during and after rain events) were collected using ISCO 6712 auto samplers. The auto samplers were programmed to collect three to eight water samples throughout each storm event depending on the duration of storm events. The samplers were programmed 24 h before the forecasted storm events to take two samples at 12 h intervals before the storm events and three-hr intervals during the storms. Two samples collected prior to the storm events were used as baseflow water samples unless the storm started before the forecasted time; in this case, one or two samples were included with the stormwater samples. This 24 h window increased our chance to capture the first stormwater rainfall flush. Stormwater sampling using autosamplers was conducted from May to December. 2014. Baseflow water was sampled biweekly from May to November in 2014, March to May in 2015, and once a month from December 2014 to February 2015. Water samples were acidified immediately in the field for subsequent TP analyses, as described above. We calculated daily external P loadings (kg/d) using measured P concentrations (mg/L) in each inflow channel and the daily discharge (L/s). Daily loadings (kg/d) for non-sampled dates were linearly interpolated using gathered data from sampling dates in R with the zoo package. We used daily mean stream flow values from USGS streamgage locations to calculate daily discharge in each lake’s watershed using a regression based drainage-area ratio method (Emerson et al., 2006). Daily external P loadings from May 2014-May 2015 (365 days) were summated to estimate the annual P loading (kg/yr). 2.1.3. Quantification of internal P loadings Quantifying internal loading, although difficult, can be done in several ways (Nürnberg, 1987). In this study, internal P load of each lake was estimated based on Nürnberg (2009). This method includes three components: 1) P release rate (g/m2 /hr) measured by flow-through experiments under aerobic and anaerobic conditions, 2) duration (days) of anoxia or aerobic conditions in the sediment, and 3) lake sediment area. To conduct the flow-through experiment, we collected seven to nine replicated sediment cores using an acryl cylinder coring device at each of the study reservoir. The sediment cores were collected on two separate occasions to represent strong stratification with anoxic sediment (July 2014) and lake turn over with aerobic sediment (Oct 2014). The collected cores were immediately moved to the lab to be used for flow-through internal loading experiments. The flow-through experiment was conducted by placing the cores (8 cm in diameter) in a water bath kept at a relatively constant room temperature. During the flow-through experiment, each core received 1 ml/min flow rate of water collected from its respective lake. We mimicked sediment anaerobic conditions in summer (i.e. stratified lakes) by purging nitrogen into inflow water. Ultrapure nitrogen gas was constantly added through tygon hose to the bottom of the inflow water jar with high pressure to bubbles the surface water (at 20–50 psi). Aerobic conditions were maintained in October cores (i.e., well-mixed lakes) by aerating the inflow water. During the flow-through experiments, dissolved oxygen (DO, mg/L) was measured in the inflow and outflow waters of each core using an YSI-556 MPS at 3–24 h intervals. Dissolved oxygen (DO) in the cores during the experiments reached below 2.0 mg/L during anaerobic conditions whereas DO ranged 8.6 − 9.8 mg/L under aerobic conditions in October (Song and Burgin, 2017). Inflow and outflow water samples were collected at 3 − 24 h intervals for 14–16 days (up to 384 h). Precise estimation of internal P loads were conducted by frequent water samplings and 4–6 replicates in the incubation experiment. Water samples were filtered immediately through 0.45 m filters and analyzed via Flow Injection Analyzer (Astoria Pacific A2) for inorganic P concentrations using the molybdate blue colorimetric method (USEPA 1993,
Please cite this article in press as: Song, K., et al., Relative importance of external and internal phosphorus loadings on affecting lake water quality in agricultural landscapes. Ecol. Eng. (2017), http://dx.doi.org/10.1016/j.ecoleng.2017.06.008
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Table 1 Physical and chemical characteristics of the study reservoirs and the surrounding landscapes. Reservoirs
Surface area (km2 )
Max. depth (m)
Max. V (m3 )
Watershed area (km2 )
Trophic Status
Bluestem Congestoga WagonTrain Yankee Hill
3.3 2.3 3.2 2.1
4.6 4.9 4.9 4.3
2,450,679 1,960,677 3,033,466 1,820,393
31.3 38.76 31.05 22.36
Hypereutrophic Hypereutrophic Hypereutrophic Hypereutrophic
Fig. 1. Temporal changes of TP in the epilimnion in the four hypereutrophic study reservoirs based on biweekly (Jun–Nov 2014) water samples.
Method 365.1). Song and Burgin (2017) described more detailed sediment core incubation technique and results. The amount of P release (or retention) was calculated by the difference of P concentrations in the outflow from the inflow (Eq. (1)).
t=T
InternalPload =
t=0
[Pt ] out − [Pt ] in T ×A
(1)
In this equation,[Pt ] out and [Pt ] in are TP concentrations from the outflow and inflow samples at a sampling time, t (hr). T represents the total incubation hours (310–384 h) for each flow-through experiment and A indicates the surface area of the sediment core (m2 ). Positive values indicate internal P loading occurs in the sediment whereas negative values signify P retention, reducing overall P concentrations in the water column. The duration of stratification or mixing (i.e. whether sediment stays anaerobic or aerobic) was determined using dissolved oxygen measurements in the water columns of each lake. DO concentration was measured biweekly at a depth interval of 0.5 m from the surface water to 0.5–1.0 m above the sediment. DO concentrations during non-sampled dates were linearly interpolated using the R package zoo. We counted days when DO in the bottom water column stayed below 2 mg/L for stratified (i.e. anaerobic) days while aerobic and mixed days were assumed to be the days making up rest of a year. Internal P load or retention under anaerobic or aerobic conditions multiplied by the duration of stratification or mixed days are then applied to the lakes total surface area (m2 ). This determines annual internal P load and retention in each reservoir. 3. Results All study reservoirs were hypereutrophic, with epilimnion TP concentrations ranging from 89 to 1052 g/L (Fig. 1). Yankee Hill and Wagon Train were more eutrophic, whereas Conestoga and Bluestem had relatively lower TP concentrations (Fig. 1). The TP concentrations in the lakes varied temporally with the highest TP concentrations in late spring and the lowest in the summer. TP concentrations from inlet streams (sources of water and TP
for the lakes) were more variable than within lake TP concentrations (Fig. 2). Spring TP was highest, reaching 1.3-2.7 (mg/L). The spring peak lasted <14 days and dropped to around 0.1-0.5 (mg/L) where they remained until late summer. This temporal variation of P concentrations was similar in every inflow channel feeding the reservoirs, and often closely followed the patterns of water discharge (Q) (Fig. 2, insets). Weekly dissolved oxygen profiles indicated that all four reservoirs experienced stratification and turnover during this study (Fig. 3). The lakes remained completely mixed until late June, at which time the surface sediment stayed aerobic with DO contents ranging from 10.7 to 4.9 (mg/L). DO in hypolimnion water gradually decreased to 0.20 (mg/L) in the late summer. From September onwards, the lakes were mixed entirely again. Stratification in each study lake persisted up to 36–60 days in 2014. Wagon Train maintained stratification for 60 days, the longest total amount of stratified days among all of the study lakes (Table 2). During this period, vertical DO differences over 5.0 (mg/L) (up to 12.6 mg/L) were consistently observed between the epilimnion and hypolimnion. We quantified internal loading during two conditions, aerobic and anaerobic using flow-through experiments. Oxygen availability altered internal P dynamics (i.e. release and retention) rates and amounts (Fig. 4). Bluestem and Conestoga released P from anaerobic sediments (Fig. 4A). Conestoga showed the highest P release rate, 36.2 g m−2 h−1 under anaerobic conditions. Aerobic conditions in post turnover reversed P dynamics in the sediment of Bluestem and Conestoga; both lakes retained P at a rate of 423.0 and 147.6 g m−2 h−1 in the sediment, respectively. Wagon Train behaved differently than Bluestem and Conestoga, showing P release under aerobic conditions (Fig. 4B). Aerobic sediment released P (2 g m−2 h−1 ) and the difference from P retention rate under anaerobic conditions was 195 g m−2 h−1 . The sediment in Yankee Hill retained P despite the sediment redox status. The release rates for internal and external loadings were applied to estimate daily loadings under anaerobic and aerobic conditions (Fig. 5). During stratified conditions (anaerobic) in the summer, internal loadings to Bluestem and Conestoga exceeded their external loads. Internal P loading in Conestoga was ∼3 kg/d, with an external load contribution of under 1 kg/d. However, when lakes were well-mixed (aerobic) in the fall, external loadings were larger than internal loadings in all four lakes. During this time, internal loading contributed to under 1 kg/d of P loading in Wagon Train, with all other lakes retaining P in the sediment. Internal and external P loadings were estimated for each of the lakes throughout the year (Table 2). When release rates from each lake are combined into a single value for external and internal loading, external loading makes up the majority of the lake’s P contributions (Fig. 6). External P loadings are 8–22 times greater than internal loadings in all four lakes. Over the course of a year, the lakes received 506–1022 kg/yr of P from nearby stream channels (Table 2), with these external loads accounting for up to 96% of total P input (Table 2 and Fig. 6). Internal P loads contributed to 4 − 12% of the total P loads (Table 2). Conestoga had the largest amount of internal P load relative to its external load at 14% (Fig. 6). Over 71 kg of P was released from sediment in stratified Bluestem and Conestoga during the summer. Wagon Train released 47 kg of
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Fig. 2. Temporal variations of TP concentration in each inflow stream channels (May 2014–May 2015). Small figures present daily discharge rate (Q, L/s) at the same inflow stream channels for four study reservoirs, A) Bluestem, B) Conestoga, C) WagonTrain and D) YankeeHill.
Table 2 Estimated duration of stratification and mixing period of each study lake and P loadings. Reservoirs
Stratified days (d)
Mixed days (d)
Internal P loading (kg/y)
External P loading (kg/y)
Bluestem Conestoga WagonTrain Yankee Hill
48 36 60 51
317 329 305 314
86.89 71.97 47.17 Retention
847 591 1022 506
P under aerobic conditions over a 305-day period in 2014 (Table 2). Yankee Hill had P retention in the sediment during both aerobic and anaerobic conditions, resulting in being an internal P sink (i.e. negative internal P loads). 4. Discussion Agricultural reservoirs, originally constructed for water storage and flood control generally retain P within the watershed (Maavara et al., 2015). As excessive P exports from agricultural fields continue increasing, reservoirs can suffer from severe eutrophication and harmful algal blooms. We quantified external P loads at 506–1022 kg P/yr for four study reservoirs. Oligotrophic lakes, with water column TP of <10 g P/L, have the equivalent of 23 kg P in the water column of an average sized Nebraskan reservoir (Carlson, 1977; Galvez-Cloutier and Sanchez, 2007). This calculation indicates that the reservoirs received 20–45 times more P annually than what a similarly size oligotrophic lake would contain. Total P concentrations in the inlet streams are greatest during high discharge storm events, particularly in spring. Previous studies reported that over 80% of the annual external P loading is related
to spring storm events (Carpenter et al., 2015; Royer et al., 2006; Sharpley and Kleinman, 1998). More soil erosion and limited nutrient uptake related to the lack of crop coverage in the spring also contributes to high TP concentrations in the water (Frost et al., 2015; Kleinman et al., 2011; Quinton et al., 2010). The temporal variation of epilimnion P concentrations in the study reservoirs reflects a similar temporal pattern found in the external P loadings (Figs. 1 and 2). The overwhelming influence of external loadings on water quality suggests that non-point source pollution control to reduce external loadings is much more likely to result in improved water quality than focusing on internal P loading control. Non-point source pollution can be limited through watershed management techniques, such as stream rehabilitation, buffer strips, constructed wetlands, and the implementation of farmer’s best management practices (Carpenter and Lathrop, 1999; Carpenter et al., 1999; Maxted et al., 2009; Pennington et al., 2003; Walsh et al., 2005). Many previous studies hypothesized that sediments in eutrophic lakes likely lose P retention capacity and that the P enriched sediment poses a high risk of being a P source (Riley and Prepas, 1984; Søndergaard et al., 1999). However, in this study, we found that the reservoirs, even under hypereutrophic con-
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Fig. 3. Isopleth diagram showing seasonal variation in dissolved oxygen (mg/L) as functions of depth in four study reservoirs.
ditions, retained P, especially when reservoirs were well mixed (i.e. aerobic conditions) (Fig. 4). Phosphorus was likely retained through the burial of algal detritus after algal blooms in the summer (Gächter and Müller, 2003; Hupfer and Lewandowski, 2008; Song and Burgin, 2017) or oxygen sensitive Fe oxide-P interaction. Aerobic sediment retains P by high adsorption capacity of FeOOH, whereas anaerobic conditions release previously sorbed P into overlying waters (Azzoni et al., 2005; Mortimer, 1942; Petticrew and Arocena, 2001). Additionally, continuously high TP concentration in water columns of the study reservoirs with high external loadings may inhibit internal P loadings.Yankee Hill where TP concentrations in water columns were relatively higher, retained P under both aerobic and anaerobic conditions (Fig. 1). This result confirms the importance that the equilibrium of P between the water column and the sediment has on internal P dynamics (Reddy et al., 2007;
Schippers et al., 2006). Higher TP concentrations in Yankee Hill (Fig. 1) resulted in high primary productivity with the average Chla concentration of 430 g/L, significantly higher than other lakes (Song and Burgin, 2017). High productivity in Yankee Hill allows sediment to contain more stable P fractions (i.e. Ca-binding P) (Song and Burgin, 2017) and prolongs aerobic conditions throughout the year (Fig. 3), both of which likely suppress internal P loadings (Søndergaard et al., 2003). The majority of internal P loading (i.e. P release from sediment) occurred in the summer when reservoirs experience strong stratification (i.e. anaerobic conditions). This is likely associated with oxygen availability in the sediments and chemical dissolution of P (Azzoni et al., 2005; Mortimer, 1942; Petticrew and Arocena, 2001). Internal P loadings, found in Bluestem and Conestoga during the summer, were estimated to be 72–87 kg/y and account for 9 and 11% of total P input, respectively. Despite a limited contribution of internal P loads to total P input
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Fig. 4. Averaged P release/retention rate (g/m2 /hr) during flow-through experiments conducted under anaerobic (A) and aerobic (B) conditions.
Fig. 5. Estimation of daily external (A) and internal (B) loadings (kg/d) under anaerobic and aerobic conditions. Internal P retention was presented as Ret, instead of actual value.
Fig. 6. Relative contribution of annual external (grey) and internal P (black) loads into total P input to the study reservoirs.
in the reservoirs, the internal P loads in the summer exceeded the external P loads during this period (Fig. 5). Our results suggest the high potential of internal P loads as an additional P source. Given that the internal P loadings occur in the summer as the same time or prior to algal blooms, additional P input from internal loadings following external loads in the spring, likely worsen eutrophication and algal blooms.
We recognize the limitation and uncertainty of our loading estimations. For example, variability of water samples, different methods between internal and external load, and linear interpolation between samples to fill in missing data points increase the uncertainty of P load estimation (Johnes, 2007; Nürnberg, 1987). For internal P loads, we reduced the uncertainty of the estimation by conducting the flow-through sediment incubation in both aerobic and anaerobic conditions to better represent natural lake sediment conditions throughout a year as suggested in a previous study (Nürnberg, 2009). However, errors still arise as anaerobic and aerobic conditions were determined at the deepest location in each reservoir, which did not represent spatial heterogeneity of oxygen availability in the sediment. Despite the uncertainties of our estimations, our findings are novel as we quantified both internal and external P loads and compared their relative importance on affecting water quality in the reservoirs. Our study, thus, can advance the understanding of P dynamics in agricultural watersheds and reservoirs. In this study, we found that external P carried by runoff from watersheds was still the dominant source of P, contributing up to 96% of the total P input to the study reservoirs. Internal P loadings accounted for 4–12% of the total annual P loads. During stratified conditions (anaerobic) in the summer, internal loadings exceeded external loads in two of the study lakes. Internal P loading which occurs when external P loads drop in the summer, can exacerbate and prolong algal blooms and eutrophication. Severe and prolonged
Please cite this article in press as: Song, K., et al., Relative importance of external and internal phosphorus loadings on affecting lake water quality in agricultural landscapes. Ecol. Eng. (2017), http://dx.doi.org/10.1016/j.ecoleng.2017.06.008
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eutrophication in agricultural reservoirs likely release high P in the outflow channels, and in turn negatively affect downstream water quality and aquatic communities in the summer. Therefore, the timing of both internal and external P loadings should be considered during water quality management. A combined approach that uses both in-lake restoration and watershed management will ensure a reduction in the amount of overall P inputs and better water quality in agricultural reservoirs and downstream ecosystems.
Acknowledgements This study was funded by Nebraska Department of Environmental Quality. We also thank to David Moscicki, Cain Silvey and Carrie Adkisson for their field and laboratory support. Publication was assisted by U.S. National Science Foundation grant number 1619948 with project title: U.S. Science International Collaborations and Contributions to EcoSummit 2016 “Sustainability: Engineering Change”
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Relative importance of external and internal phosphorus loadings on affecting lake water quality in agricultural landscapes Keunyea Song a,∗ , Craig J. Adams b , Amy J. Burgin a a b
University of Kansas and Kanas Biological Survey, University of Kansas, 2101 Constant Ave., Lawrence, KS, 66047 USA School of Natural Resources, University of Nebraska-Lincoln, 3310 Holdrege Street, Lincoln, NE, 68583 USA
a r t i c l e
i n f o
Article history: Received 31 March 2017 Received in revised form 5 June 2017 Accepted 5 June 2017 Available online xxx Keywords: Agricultural reservoir Eutrophication External P loading Internal P loading Flow-through sediment core incubation
a b s t r a c t Internal phosphorus (P) loading from the sediment poses a high risk of being an additional P source to deteriorate water quality. Previous studies hypothesized that internal P loads can be as high as external P inputs, especially in P enriched landscapes such as agricultural areas. However, internal P loadings in eutrophic conditions are rarely quantified or compared with external P loads. In this study, we aimed to answer these three questions; 1) how much P is internally released from the sediment of hypereutrophic lakes? 2) how much do internal P loads contribute to lake water quality compared to external loads? and 3) what factors regulate the release and retention of P in the sediment? We selected four hypereutrophic lakes located in Eastern Nebraska. In the study lakes and watersheds, internal and external P loads were quantified in 2014. Total P concentrations of inflow water collected from primary water channels feeding the study lakes and daily inflow water discharge rates were used to calculate external P loads. Internal P loads were quantified from flow-through soil core incubation experiments. External TP loads varied temporarily depending on the changes in discharge, and were highest during spring storm events. The majority of internal P loading (i.e. P release from sediment) occurred in the summer when lakes experience strong stratification (i.e. anaerobic conditions). This is likely associated with oxygen availability in the sediments and chemical dissolution of P. By comparing the annual-scale of external and internal P inputs, external P loadings were still the dominant P source to the lakes, contributing up to 98% of the total P input whereas internal P loadings accounted for 4–12% of the total P input. Although internal P loads were relatively minor on an annual time scale, we found that summer internal loadings in some of study lakes exceeded their external loadings. Our results confirmed the dominant influence of external P loadings on water quality in the reservoirs. This suggests that non-point source controls and watershed management strategies to reduce external loadings should be implemented prior to internal P loading controls. Internal P loadings can be a significant P source, even if just temporarily, worsening water quality of agricultural reservoirs and downstream ecosystems in the summer. © 2017 Elsevier B.V. All rights reserved.
1. Introduction Eutrophication is one of the most common water quality problems in the world. Nearly half of all US lakes are impaired by eutrophication, mainly from excessive phosphorus (P) loading (Carpenter et al., 1999; Dodds et al., 2009; Smith and Schindler, 2009). Eutrophication results in harmful algal blooms, hypoxia in coastal areas and loss of biodiversity. Such water quality deterioration is estimated to cause an annual loss of approximately $ 2.2 billion in the US (Dodds et al., 2009).
∗ Corresponding author. E-mail address: [email protected] (K. Song).
Agricultural activity is one of the major contributors of P to aquatic ecosystems (Kleinman et al., 2011; Royer et al., 2006; Schippers et al., 2006). The use of P in agricultural fertilizer has increased 3.5 times since 1960 and is expected to continue increasing (Smil, 2000; Tilman et al., 2001). Phosphorus is a necessary nutrient for crop production, and also the limiting nutrient for primary productivity in freshwater (Elser et al., 2007; Smil, 2000; Smith and Schindler, 2009). Phosphorus carried with water through rivers and stream channels in watersheds to downstream, lakes or reservoirs, is called external P loading. Variation in external P loading to lakes is driven by the timing of fertilizer application, crop production, soil type, and rainfall patterns (Royer et al., 2006). Once P enters into lakes, it can go through an internal cycle within foodwebs or be retained in the sediment, which accumulates over time, creating P and organic matter enriched sediment (Das et al., 2012;
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Søndergaard et al., 1993). Inorganic P can be chemically bound and deposited in sediments. Sediments also contain high loads of organic or particulate P, which can be released from decomposition (Song and Burgin, 2017). Sediment P concentrations can be 100X higher than water column concentrations, especially when excessive external P loads persist over time, such as in agricultural watersheds (Diaz et al., 2006; Reddy et al., 1999). Phosphorus enriched sediment is problematic because sediment P can be released back into the water column, a phenomenon termed internal loading. Lack of oxygen, pH changes, or decomposition can trigger internal P loading (Hupfer and Lewandowski, 2008; Jensen and Andersen, 1992; Pettersson, 1998). For example, in summer when strong stratification prevents the vertical exchange of materials in lakes and creates hypoxia in the sediment, chemically bound P is released (Nürnberg, 1987; Pettersson, 1998). Decomposition, mainly under aerobic conditions breaks down organic matter and releases inorganic or dissolved organic P into water columns (Hupfer and Lewandowski, 2008; Song and Burgin, 2017). As lakes eutrophy, internal P loading becomes a potentially large P source compared to external P loading (Coveney et al., 2005; Hamilton, 2012). Despite the potential for internal P loading to deteriorate water quality, especially in eutrophic or hypereutrophic lakes, internal P loading is rarely quantified and directly compared to external P loading. Therefore, we asked: 1) How much P is internally released from the sediment of hypereutrophic lakes? 2) How much do internal P loads contribute to lake water quality compared to external loads? and 3) What factors regulate the release and retention of P in the sediment? To answer these questions, we quantified both internal and external P loads in four hypereutrophic lakes within agricultural landscapes. Flow-through sediment core incubation experiments under anaerobic and aerobic conditions to quantify internal P loadings. 2. Materials and methods 2.1. Site description We selected four lakes located in Eastern Nebraska for this study. The study lakes (Table 1) were constructed in the 1960s primarily for water storage and have been restored through sediment dredging and watershed management in the last 20 years. All study reservoirs have similar morphological characteristics-surface area, water depth, and surrounding landscapes (Table 1). Agricultural areas make up 50–75% of their watersheds. All of them are considered to be in eutrophic-hypereutrophic states, as indicated by chlorophyll-a contents and total phosphorus (TP) concentrations in summer (Song and Burgin, 2017). 2.1.1. Lake water quality monitoring Water samples were collected biweekly at the deepest locations from the epilimnion using a Van Dorn sampler. A Garmin Legend CX-GPS was used for positioning to ensure samples were consistently collected from the same locations. Water sampling was conducted from June to Nov. 2014. Collected water samples were acidified immediately in the field. The samples were then digested in the laboratory using potassium persulfate and analyzed via a Flow Injection Analyzer (Astoria Pacific A2) for TP concentrations using the molybdate blue colorimetric method (USEPA 1993, Method 365.1). 2.1.2. Quantification of external P loadings Inflow water samples from primary water channels feeding the study lakes were collected through baseflow water sampling and stormwater sampling. Baseflow water samples (flow during
dry weather conditions) were gathered biweekly by grab sampling. Storm water samples (flow during and after rain events) were collected using ISCO 6712 auto samplers. The auto samplers were programmed to collect three to eight water samples throughout each storm event depending on the duration of storm events. The samplers were programmed 24 h before the forecasted storm events to take two samples at 12 h intervals before the storm events and three-hr intervals during the storms. Two samples collected prior to the storm events were used as baseflow water samples unless the storm started before the forecasted time; in this case, one or two samples were included with the stormwater samples. This 24 h window increased our chance to capture the first stormwater rainfall flush. Stormwater sampling using autosamplers was conducted from May to December. 2014. Baseflow water was sampled biweekly from May to November in 2014, March to May in 2015, and once a month from December 2014 to February 2015. Water samples were acidified immediately in the field for subsequent TP analyses, as described above. We calculated daily external P loadings (kg/d) using measured P concentrations (mg/L) in each inflow channel and the daily discharge (L/s). Daily loadings (kg/d) for non-sampled dates were linearly interpolated using gathered data from sampling dates in R with the zoo package. We used daily mean stream flow values from USGS streamgage locations to calculate daily discharge in each lake’s watershed using a regression based drainage-area ratio method (Emerson et al., 2006). Daily external P loadings from May 2014-May 2015 (365 days) were summated to estimate the annual P loading (kg/yr). 2.1.3. Quantification of internal P loadings Quantifying internal loading, although difficult, can be done in several ways (Nürnberg, 1987). In this study, internal P load of each lake was estimated based on Nürnberg (2009). This method includes three components: 1) P release rate (g/m2 /hr) measured by flow-through experiments under aerobic and anaerobic conditions, 2) duration (days) of anoxia or aerobic conditions in the sediment, and 3) lake sediment area. To conduct the flow-through experiment, we collected seven to nine replicated sediment cores using an acryl cylinder coring device at each of the study reservoir. The sediment cores were collected on two separate occasions to represent strong stratification with anoxic sediment (July 2014) and lake turn over with aerobic sediment (Oct 2014). The collected cores were immediately moved to the lab to be used for flow-through internal loading experiments. The flow-through experiment was conducted by placing the cores (8 cm in diameter) in a water bath kept at a relatively constant room temperature. During the flow-through experiment, each core received 1 ml/min flow rate of water collected from its respective lake. We mimicked sediment anaerobic conditions in summer (i.e. stratified lakes) by purging nitrogen into inflow water. Ultrapure nitrogen gas was constantly added through tygon hose to the bottom of the inflow water jar with high pressure to bubbles the surface water (at 20–50 psi). Aerobic conditions were maintained in October cores (i.e., well-mixed lakes) by aerating the inflow water. During the flow-through experiments, dissolved oxygen (DO, mg/L) was measured in the inflow and outflow waters of each core using an YSI-556 MPS at 3–24 h intervals. Dissolved oxygen (DO) in the cores during the experiments reached below 2.0 mg/L during anaerobic conditions whereas DO ranged 8.6 − 9.8 mg/L under aerobic conditions in October (Song and Burgin, 2017). Inflow and outflow water samples were collected at 3 − 24 h intervals for 14–16 days (up to 384 h). Precise estimation of internal P loads were conducted by frequent water samplings and 4–6 replicates in the incubation experiment. Water samples were filtered immediately through 0.45 m filters and analyzed via Flow Injection Analyzer (Astoria Pacific A2) for inorganic P concentrations using the molybdate blue colorimetric method (USEPA 1993,
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Table 1 Physical and chemical characteristics of the study reservoirs and the surrounding landscapes. Reservoirs
Surface area (km2 )
Max. depth (m)
Max. V (m3 )
Watershed area (km2 )
Trophic Status
Bluestem Congestoga WagonTrain Yankee Hill
3.3 2.3 3.2 2.1
4.6 4.9 4.9 4.3
2,450,679 1,960,677 3,033,466 1,820,393
31.3 38.76 31.05 22.36
Hypereutrophic Hypereutrophic Hypereutrophic Hypereutrophic
Fig. 1. Temporal changes of TP in the epilimnion in the four hypereutrophic study reservoirs based on biweekly (Jun–Nov 2014) water samples.
Method 365.1). Song and Burgin (2017) described more detailed sediment core incubation technique and results. The amount of P release (or retention) was calculated by the difference of P concentrations in the outflow from the inflow (Eq. (1)).
t=T
InternalPload =
t=0
[Pt ] out − [Pt ] in T ×A
(1)
In this equation,[Pt ] out and [Pt ] in are TP concentrations from the outflow and inflow samples at a sampling time, t (hr). T represents the total incubation hours (310–384 h) for each flow-through experiment and A indicates the surface area of the sediment core (m2 ). Positive values indicate internal P loading occurs in the sediment whereas negative values signify P retention, reducing overall P concentrations in the water column. The duration of stratification or mixing (i.e. whether sediment stays anaerobic or aerobic) was determined using dissolved oxygen measurements in the water columns of each lake. DO concentration was measured biweekly at a depth interval of 0.5 m from the surface water to 0.5–1.0 m above the sediment. DO concentrations during non-sampled dates were linearly interpolated using the R package zoo. We counted days when DO in the bottom water column stayed below 2 mg/L for stratified (i.e. anaerobic) days while aerobic and mixed days were assumed to be the days making up rest of a year. Internal P load or retention under anaerobic or aerobic conditions multiplied by the duration of stratification or mixed days are then applied to the lakes total surface area (m2 ). This determines annual internal P load and retention in each reservoir. 3. Results All study reservoirs were hypereutrophic, with epilimnion TP concentrations ranging from 89 to 1052 g/L (Fig. 1). Yankee Hill and Wagon Train were more eutrophic, whereas Conestoga and Bluestem had relatively lower TP concentrations (Fig. 1). The TP concentrations in the lakes varied temporally with the highest TP concentrations in late spring and the lowest in the summer. TP concentrations from inlet streams (sources of water and TP
for the lakes) were more variable than within lake TP concentrations (Fig. 2). Spring TP was highest, reaching 1.3-2.7 (mg/L). The spring peak lasted <14 days and dropped to around 0.1-0.5 (mg/L) where they remained until late summer. This temporal variation of P concentrations was similar in every inflow channel feeding the reservoirs, and often closely followed the patterns of water discharge (Q) (Fig. 2, insets). Weekly dissolved oxygen profiles indicated that all four reservoirs experienced stratification and turnover during this study (Fig. 3). The lakes remained completely mixed until late June, at which time the surface sediment stayed aerobic with DO contents ranging from 10.7 to 4.9 (mg/L). DO in hypolimnion water gradually decreased to 0.20 (mg/L) in the late summer. From September onwards, the lakes were mixed entirely again. Stratification in each study lake persisted up to 36–60 days in 2014. Wagon Train maintained stratification for 60 days, the longest total amount of stratified days among all of the study lakes (Table 2). During this period, vertical DO differences over 5.0 (mg/L) (up to 12.6 mg/L) were consistently observed between the epilimnion and hypolimnion. We quantified internal loading during two conditions, aerobic and anaerobic using flow-through experiments. Oxygen availability altered internal P dynamics (i.e. release and retention) rates and amounts (Fig. 4). Bluestem and Conestoga released P from anaerobic sediments (Fig. 4A). Conestoga showed the highest P release rate, 36.2 g m−2 h−1 under anaerobic conditions. Aerobic conditions in post turnover reversed P dynamics in the sediment of Bluestem and Conestoga; both lakes retained P at a rate of 423.0 and 147.6 g m−2 h−1 in the sediment, respectively. Wagon Train behaved differently than Bluestem and Conestoga, showing P release under aerobic conditions (Fig. 4B). Aerobic sediment released P (2 g m−2 h−1 ) and the difference from P retention rate under anaerobic conditions was 195 g m−2 h−1 . The sediment in Yankee Hill retained P despite the sediment redox status. The release rates for internal and external loadings were applied to estimate daily loadings under anaerobic and aerobic conditions (Fig. 5). During stratified conditions (anaerobic) in the summer, internal loadings to Bluestem and Conestoga exceeded their external loads. Internal P loading in Conestoga was ∼3 kg/d, with an external load contribution of under 1 kg/d. However, when lakes were well-mixed (aerobic) in the fall, external loadings were larger than internal loadings in all four lakes. During this time, internal loading contributed to under 1 kg/d of P loading in Wagon Train, with all other lakes retaining P in the sediment. Internal and external P loadings were estimated for each of the lakes throughout the year (Table 2). When release rates from each lake are combined into a single value for external and internal loading, external loading makes up the majority of the lake’s P contributions (Fig. 6). External P loadings are 8–22 times greater than internal loadings in all four lakes. Over the course of a year, the lakes received 506–1022 kg/yr of P from nearby stream channels (Table 2), with these external loads accounting for up to 96% of total P input (Table 2 and Fig. 6). Internal P loads contributed to 4 − 12% of the total P loads (Table 2). Conestoga had the largest amount of internal P load relative to its external load at 14% (Fig. 6). Over 71 kg of P was released from sediment in stratified Bluestem and Conestoga during the summer. Wagon Train released 47 kg of
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Fig. 2. Temporal variations of TP concentration in each inflow stream channels (May 2014–May 2015). Small figures present daily discharge rate (Q, L/s) at the same inflow stream channels for four study reservoirs, A) Bluestem, B) Conestoga, C) WagonTrain and D) YankeeHill.
Table 2 Estimated duration of stratification and mixing period of each study lake and P loadings. Reservoirs
Stratified days (d)
Mixed days (d)
Internal P loading (kg/y)
External P loading (kg/y)
Bluestem Conestoga WagonTrain Yankee Hill
48 36 60 51
317 329 305 314
86.89 71.97 47.17 Retention
847 591 1022 506
P under aerobic conditions over a 305-day period in 2014 (Table 2). Yankee Hill had P retention in the sediment during both aerobic and anaerobic conditions, resulting in being an internal P sink (i.e. negative internal P loads). 4. Discussion Agricultural reservoirs, originally constructed for water storage and flood control generally retain P within the watershed (Maavara et al., 2015). As excessive P exports from agricultural fields continue increasing, reservoirs can suffer from severe eutrophication and harmful algal blooms. We quantified external P loads at 506–1022 kg P/yr for four study reservoirs. Oligotrophic lakes, with water column TP of <10 g P/L, have the equivalent of 23 kg P in the water column of an average sized Nebraskan reservoir (Carlson, 1977; Galvez-Cloutier and Sanchez, 2007). This calculation indicates that the reservoirs received 20–45 times more P annually than what a similarly size oligotrophic lake would contain. Total P concentrations in the inlet streams are greatest during high discharge storm events, particularly in spring. Previous studies reported that over 80% of the annual external P loading is related
to spring storm events (Carpenter et al., 2015; Royer et al., 2006; Sharpley and Kleinman, 1998). More soil erosion and limited nutrient uptake related to the lack of crop coverage in the spring also contributes to high TP concentrations in the water (Frost et al., 2015; Kleinman et al., 2011; Quinton et al., 2010). The temporal variation of epilimnion P concentrations in the study reservoirs reflects a similar temporal pattern found in the external P loadings (Figs. 1 and 2). The overwhelming influence of external loadings on water quality suggests that non-point source pollution control to reduce external loadings is much more likely to result in improved water quality than focusing on internal P loading control. Non-point source pollution can be limited through watershed management techniques, such as stream rehabilitation, buffer strips, constructed wetlands, and the implementation of farmer’s best management practices (Carpenter and Lathrop, 1999; Carpenter et al., 1999; Maxted et al., 2009; Pennington et al., 2003; Walsh et al., 2005). Many previous studies hypothesized that sediments in eutrophic lakes likely lose P retention capacity and that the P enriched sediment poses a high risk of being a P source (Riley and Prepas, 1984; Søndergaard et al., 1999). However, in this study, we found that the reservoirs, even under hypereutrophic con-
Please cite this article in press as: Song, K., et al., Relative importance of external and internal phosphorus loadings on affecting lake water quality in agricultural landscapes. Ecol. Eng. (2017), http://dx.doi.org/10.1016/j.ecoleng.2017.06.008
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Fig. 3. Isopleth diagram showing seasonal variation in dissolved oxygen (mg/L) as functions of depth in four study reservoirs.
ditions, retained P, especially when reservoirs were well mixed (i.e. aerobic conditions) (Fig. 4). Phosphorus was likely retained through the burial of algal detritus after algal blooms in the summer (Gächter and Müller, 2003; Hupfer and Lewandowski, 2008; Song and Burgin, 2017) or oxygen sensitive Fe oxide-P interaction. Aerobic sediment retains P by high adsorption capacity of FeOOH, whereas anaerobic conditions release previously sorbed P into overlying waters (Azzoni et al., 2005; Mortimer, 1942; Petticrew and Arocena, 2001). Additionally, continuously high TP concentration in water columns of the study reservoirs with high external loadings may inhibit internal P loadings.Yankee Hill where TP concentrations in water columns were relatively higher, retained P under both aerobic and anaerobic conditions (Fig. 1). This result confirms the importance that the equilibrium of P between the water column and the sediment has on internal P dynamics (Reddy et al., 2007;
Schippers et al., 2006). Higher TP concentrations in Yankee Hill (Fig. 1) resulted in high primary productivity with the average Chla concentration of 430 g/L, significantly higher than other lakes (Song and Burgin, 2017). High productivity in Yankee Hill allows sediment to contain more stable P fractions (i.e. Ca-binding P) (Song and Burgin, 2017) and prolongs aerobic conditions throughout the year (Fig. 3), both of which likely suppress internal P loadings (Søndergaard et al., 2003). The majority of internal P loading (i.e. P release from sediment) occurred in the summer when reservoirs experience strong stratification (i.e. anaerobic conditions). This is likely associated with oxygen availability in the sediments and chemical dissolution of P (Azzoni et al., 2005; Mortimer, 1942; Petticrew and Arocena, 2001). Internal P loadings, found in Bluestem and Conestoga during the summer, were estimated to be 72–87 kg/y and account for 9 and 11% of total P input, respectively. Despite a limited contribution of internal P loads to total P input
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Fig. 4. Averaged P release/retention rate (g/m2 /hr) during flow-through experiments conducted under anaerobic (A) and aerobic (B) conditions.
Fig. 5. Estimation of daily external (A) and internal (B) loadings (kg/d) under anaerobic and aerobic conditions. Internal P retention was presented as Ret, instead of actual value.
Fig. 6. Relative contribution of annual external (grey) and internal P (black) loads into total P input to the study reservoirs.
in the reservoirs, the internal P loads in the summer exceeded the external P loads during this period (Fig. 5). Our results suggest the high potential of internal P loads as an additional P source. Given that the internal P loadings occur in the summer as the same time or prior to algal blooms, additional P input from internal loadings following external loads in the spring, likely worsen eutrophication and algal blooms.
We recognize the limitation and uncertainty of our loading estimations. For example, variability of water samples, different methods between internal and external load, and linear interpolation between samples to fill in missing data points increase the uncertainty of P load estimation (Johnes, 2007; Nürnberg, 1987). For internal P loads, we reduced the uncertainty of the estimation by conducting the flow-through sediment incubation in both aerobic and anaerobic conditions to better represent natural lake sediment conditions throughout a year as suggested in a previous study (Nürnberg, 2009). However, errors still arise as anaerobic and aerobic conditions were determined at the deepest location in each reservoir, which did not represent spatial heterogeneity of oxygen availability in the sediment. Despite the uncertainties of our estimations, our findings are novel as we quantified both internal and external P loads and compared their relative importance on affecting water quality in the reservoirs. Our study, thus, can advance the understanding of P dynamics in agricultural watersheds and reservoirs. In this study, we found that external P carried by runoff from watersheds was still the dominant source of P, contributing up to 96% of the total P input to the study reservoirs. Internal P loadings accounted for 4–12% of the total annual P loads. During stratified conditions (anaerobic) in the summer, internal loadings exceeded external loads in two of the study lakes. Internal P loading which occurs when external P loads drop in the summer, can exacerbate and prolong algal blooms and eutrophication. Severe and prolonged
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eutrophication in agricultural reservoirs likely release high P in the outflow channels, and in turn negatively affect downstream water quality and aquatic communities in the summer. Therefore, the timing of both internal and external P loadings should be considered during water quality management. A combined approach that uses both in-lake restoration and watershed management will ensure a reduction in the amount of overall P inputs and better water quality in agricultural reservoirs and downstream ecosystems.
Acknowledgements This study was funded by Nebraska Department of Environmental Quality. We also thank to David Moscicki, Cain Silvey and Carrie Adkisson for their field and laboratory support. Publication was assisted by U.S. National Science Foundation grant number 1619948 with project title: U.S. Science International Collaborations and Contributions to EcoSummit 2016 “Sustainability: Engineering Change”
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