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The contribution of plant uptake to nutrient removal by floating treatment wetlands
Ecological Engineering 73 (2014) 684–690
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Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
The contribution of plant uptake to nutrient removal by floating treatment wetlands Hanneke E. Keizer-Vlek *, Piet F.M. Verdonschot, Ralf C.M. Verdonschot, Dorine Dekkers Department of Freshwater Ecology, Alterra, Wageningen University and Research Centre, P.O. Box 47, Wageningen 6700 AA, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 March 2014 Received in revised form 4 September 2014 Accepted 26 September 2014 Available online xxx
Floating treatment wetlands (FTWs) may provide an appealing alternative to the more conventional (sub) surface flow wetlands to solve problems associated with eutrophication in urban surface waters, because they do not claim additional land area. This study examined the contribution of plant uptake to overall removal capacity of FTWs. A batch mesocosm experiment was performed during the growing season using thirty 84 L polyethylene tanks covered with 0.28 m2 floating Styrofoam mats. Ten tanks served as a control (only Styrofoam cover), 10 tanks were planted with Iris pseudacorus, and 10 with Typha angustifolia. Nutrients were added weekly to keep total nitrogen (TN) and total phosphorous (TP) concentrations at approximately 4 mg N L 1 and 0.25 mg P L 1. Total removal of TN an TP from the treatment with Typha was relatively low, resulting from the limited increase in plant biomass during the experiment. Total removal of TN and TP from the tanks planted with Iris was 277 mg N m 2 d 1 and 9.32 mg P m 2 d 1 during the experiment. These values were significantly higher than the values for total removal from the control tanks, i.e., 54 times higher for TN removal and 10 times higher for TP removal. Plant uptake played a major role in the removal of nitrogen and phosphorous from the water by FTWs, i.e., 74% of TN removal and 60% of TP removal resulted from Iris uptake. These results suggest that FTWs planted with Iris can be applied in a temperate climate to overcome problems with excessive algae growth in surface waters. ã 2014 Elsevier B.V. All rights reserved.
Keywords: Floating treatment wetland Plant biomass production Nutrient removal Eutrophication Typha angustifolia Iris pseudacorus
1. Introduction Human-induced eutrophication threatens the ecological quality of freshwater ecosystems worldwide. The problems associated with eutrophication are excessive macrophyte/algae growth resulting in oxygen depletion, stench, and fish mortality. Furthermore, the growth of toxin-excreting blue-green algae poses problems for human health. A popular way of reducing the nutrient loading to surface waters has been the construction of (sub) surface flow wetlands to treat different types of wastewater, including municipal wastewater, acid mine drainage, industrial wastewater, agricultural and storm water runoff, as well as effluent from livestock operations (Lin et al., 2002a,b,b). The advantages of (sub) surface flow constructed wetlands are moderate capital costs, very low energy consumption and maintenance requirements, and benefits of increased wildlife habitat (International
* Corresponding author. Tel.: +31 317 486423; fax: +31 317 419000. E-mail addresses: [email protected] (H.E. Keizer-Vlek), [email protected] (P.F.M. Verdonschot), [email protected] (R.C.M. Verdonschot), [email protected] (D. Dekkers). http://dx.doi.org/10.1016/j.ecoleng.2014.09.081 0925-8574/ ã 2014 Elsevier B.V. All rights reserved.
Water Association (IWA), 2000). However, these conventional wetlands are not likely to be applied in situations where land area is limited, such as in large cities. Floating treatment wetlands (FTWs) might represent a solution to the problem of limited land area because the technique does not ‘claim’ any land area. In FTWs, emergent macrophytes grow on a floating mat that is placed on the water surface. In contrast to the more conventional wetland systems, the emergent macrophytes are not anchored in the sediment of the wetland, instead, their roots hang in the water column, where the plants will take up nutrients directly. Other advantages of FTWs are their ability to cope with fluctuations in water levels, their aesthetic value (especially when using flowering plants), their provision of habitat for invertebrates, fish, and birds, and the sense of green they create in the city. Apart from FTWs, many studies have shown that free-floating aquatic plants, like water hyacinth (Eichhornia crassipes), water lettuce (Pistia stratiotes), and duckweed (Lemnaceae), can reduce nutrient concentrations in wastewater (see Hubbard, 2010, for an overview). However, because of their great colonization capacity, these species are often considered a nuisance in temperate waters, i.e., the large amounts of decomposing plant material will reduce oxygen concentrations in the
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water, resulting in fish kills and stench, they outcompete indigenous species, and large amounts of plant material will result in a diminished capacity of waterways to drain water. FTWs are being applied in various situations worldwide (Hu et al., 2010). The main applications of FTWs in terms of water quality improvement include the treatment of storm water, sewage, pond water, urban lake water, dairy manure effluent, and water supply reservoirs (Weragoda et al., 2012). A high number of studies have provided nutrient removal efficiencies for FTWs (e.g., Revitt et al., 1997; De Stefani et al., 2011; Vymazal, 2007). Different biological and physico–chemical processes play a role in nutrient removal using FTWs (e.g., nitrification, denitrification, P adsorption). However, the effect of the vegetation on overall removal performance is poorly documented (Chang et al., 2013; Van de Moortel et al., 2010). Therefore, the objective of this study was (1) to quantify the removal capacity for nitrogen and phosphorus of FTWs planted with Iris pseudacorus L. and Typha angustifolia L., respectively, and (2) to quantify the contribution of plant uptake to overall removal capacity of FTWs. 2. Methods 2.1. Experimental set-up A batch mesocosm experiment was carried out between May 30 and August 29 of 2012 in two horticultural polytunnels (5 m 8 m). Weather conditions during the experiment are presented in Table 1. Experiments were carried out in thirty 84 L polyethylene tanks with a surface opening of 0.28 m2. The tanks were placed in the tunnels according to a randomized block design (Fig. 1). Ten tanks served as a control, ten tanks were planted with Iris, and ten tanks were planted with Typha. On May 28, the tanks were filled with 70 L of groundwater from the well Nergena in Wageningen and covered with floating mats of Styrofoam 4 cm thick. After two days, the tanks were spiked with 1 mL Pokon (commercially available fertilizer for pot plants, universeel plantenvoeding, manufacturer Pokon Naturado) and 10 mL KNO3 solution. Twelve holes of approximately 2 cm 2 cm were cut in each Styrofoam cover. The next day, 100 mL water samples were collected from each tank for laboratory analysis of total nitrogen (TN) and total phosphorous (TP) in unfiltered samples by Chemisch Biologisch Laboratorium Bodem, accredited according to NEN-ENISO/IEC 17025 standard (registration number RvA L342). Prior to sampling, the biofilm attached to the walls and deposits on the bottom of the tank were brought into suspension. Additionally, two groundwater samples were collected and analyzed for TN and TP concentrations. Average nutrient concentrations in the tanks after the first nutrient additions are provided in Table 2. On June 4 and 5, 10 tanks were planted with Iris and 10 tanks were planted with Typha. The plants were supplied by Moerings B. V. in Roosendaal. The seed-raised plants were removed from their potting media by rinsing with water and placed in the tanks through holes in the Styrofoam. Each tank was planted with
Table 1 Weather conditions from May 30 to August 29 of 2012 at weather station De Deelen in the Netherlands (Source: KNMI). Variable
Value
Average temperature ( C) Average minimum temperature( C) Average maximum temperature ( C) Total rainfall (mm) Hours of sunshine Number of days without rainfall Number of days with a maximum temp of 25 C or higher
16.6 11.5 21.5 294 553 34 16
685
Fig. 1. Photo of the experimental set-up.
12 specimens of one of the two species. The Typha plants were secured to a cocktail stick pinned in the Styrofoam. From the supplied batch of plants, 12 random specimens of Iris and Typha, respectively, were kept separate to determine plant biomass (dry weight) and TN and TP tissue concentrations at the start of the experiment. NH4–N, NO2 + NO3–N, and PO4–P concentrations were monitored weekly during the experiment to avoid nutrient deficiencies in the plants arising from low nutrient concentrations in the water because of removal processes. For this purpose, a 100 mL water sample was collected weekly from a randomly selected tank of each treatment. Each week, three different tanks were sampled. Based on measured nutrient concentrations, additions of Pokon and KNO3 were made to maintain a minimum concentration of approximately 4 mg N L 1 and 0.25 mg P L 1. As a result, total nutrient additions varied depending on the treatment (Table 3). Additions with Pokon ensured the presence of trace elements (K, Fe, Mn, B, Cu, Zn, and Mo). When water levels dropped below 40 L because of evaporation and transpiration, groundwater from the well Nergena was used to top up the water level in the tanks. After 91 days, water volume in the tanks was determined. Water samples of 100 mL were collected from each tank for laboratory analysis of nutrients (TN and TP). All plants were removed from the tanks to determine plant biomass (dry weight) and TN and TP tissue concentrations at the end of the experiment. Floating algae were removed from the water surface using a small net to determine algae biomass (dry weight) and TN and TP tissue concentrations. 2.2. Plant sampling and analysis After removal of the plants from the tanks, the shoots were separated from the roots. The dry weight of roots and shoots was determined after drying to constant weight (at least 48 h) in a fancirculated oven at 70 C. The total biomass of shoots and roots was determined per tank (total of 12 plants). Representative dried tissue subsamples of roots and shoots were taken, ground, and analyzed for TN and TP by Chemisch Biologisch Laboratorium Bodem. The 12 Typha and Iris plants randomly collected at the start of the experiment received the same treatment as the plants Table 2 Average nutrient concentrations (standard deviation) in the tanks after the first nutrient additions. Treatment
TN (mg N L
Groundwater Control Iris Typha
0.09 0.04 3.85 0.28 3.90 0.11 4.07 0.42
1
)
TP (mg N L 0.02 0.02 0.15 0.02 0.17 0.02 0.17 0.01
1
)
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Table 3 Overview per treatment of the total amount of TN and TP added to each tank during the experiment. Treatment
TN (mg)
TP (mg)
Control Iris Typha
906 7217 1241
94 259 78
collected at the end of the experiment, except that dry weight and TN and TP tissue concentrations were determined for six of the 12 individual plants. Samples of floating algae were treated the same as the plant samples to determine dry weight and TN and TP tissue concentrations. 2.3. Removal capacity Average plant dry weight at the start of the experiment was calculated based on the 12 randomly selected plants of Iris and Typha. Total removal capacity was calculated by determining the total amount of nutrients added to each tank minus the amount of TN and TP present in the tank at the end of the experiment (TN and TP concentrations multiplied by the water volume). To determine plant uptake of nitrogen and phosphorous during the experiment, (estimated) dry weight at the start and end of the experiment was multiplied by TN and TP tissue concentrations at both time points. We did not correct for the addition of nutrients attributable to the addition of groundwater after evapotranspiration because this amount was negligible in comparison to the nutrient additions attributable to Pokon and KNO3. 2.4. Statistical analysis Statistical analyses were performed with IBM SPSS 19.0. In the case of TN removal and TP uptake by floating algae, data were distributed normally and variances were equal, so an ANOVA was performed. In cases of significant differences between treatments, the ANOVA was followed by post hoc testing using Tukey's HSD test. In all other cases, a non-parametric Kruskal–Wallis test for multiple comparisons was applied to test for differences between treatments because the data were not distributed normally and/or homogeneity of variance was lacking. When significant differences between treatments were present, Mann–Whitney U tests were performed. A Bonferroni correction was applied to overcome inflated Type I errors, reducing the level of significance to 0.05/ 3 = 0.017. During all other statistical tests, the level of significance was held at 0.05. 3. Results 3.1. Nitrogen and phosphorus removal Nutrient removal capacity for TP and TN differed significantly between the different treatments (p < 0.001). The removal of both TP and TN was lowest in the control and highest in the Iris treatment (Fig. 2). The difference between the control and Typha treatment was non-significant for TP (p = 0.315). TN removal capacity differed significantly between the Typha treatment and control (p < 0.001), but this difference was relatively small compared to that between the Iris treatment and control (Fig. 2). The removal efficiency for TN differed among all treatments (p < 0.001 for all comparisons). The removal efficiency was highest in the Iris treatment (98%), followed by the Typha treatment (57%) and the control (14%) (Table 4). This sequence can be explained by the fact that nutrient additions to the Typha treatment were far lower than nutrient additions to the Iris treatment (Table 3).
Fig. 2. Removal of TN (a) and TP (b) from the water in the tanks during the experiment (n = 10). Range bars show maximum and minimum values, boxes show interquartile ranges (25th–75th percentile), and black squares represent averages. Treatments indicated with different letters are significantly different (Tuckey post hoc comparisons, a = 0.5 for TN removal and Mann–Whitney U non-parametric post-hoc comparisons, Bonferroni corrected a = 0.017 for TP removal).
Although the TN removal efficiency in the Typha and Iris treatments was significantly higher than in the control treatment, the total amount of TN removed from the Typha treatment was relatively small compared to the Iris treatment (Fig. 2). The TP removal efficiency was significantly higher in the Iris treatment compared to the control and the Typha treatment (92% vs 23%, p < 0.001). There was no significant difference in TP removal efficiency between the control and the Typha treatment (p = 0.853). 3.2. Plant growth and uptake The average biomass (dry weight) of Iris increased threefold during the experiment, and the biomass of Typha doubled (Fig. 3). The increase in Iris biomass was mainly the result of an increase in shoot biomass while the Typha treatment showed an increase in both root and shoot biomass (Fig. 3). However, the absolute increase in biomass for Typha was low compared to Iris (Fig. 3). Table 4 Removal efficiency of TN and TP for the three treatments (n = 10). Treatments indicated with different letters are significantly different (Mann–Whitney U nonparametric post-hoc comparisons, Bonferroni corrected a = 0.017). Treatment
Control Iris Typha
Removal efficiency (%) TN
TP
14 9a 98 0.5b 57 7c
23 11a 92 2b 23 11a
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the start. For TN, this arose because of higher average root tissue concentrations at the end of the experiment. For TP, average tissue concentrations for both shoot and root declined during the experiment, however, average shoot concentrations declined more than average root concentrations (Table 5). Most remarkable were the very low TP concentrations in Iris for both roots and shoots at the end of the experiment. Average TN and TP plant uptake differed significantly between the Iris and Typha treatments (p < 0.001). Average TN and TP plant uptake in the Typha treatment was minimal (Fig. 4a), but average TN and TP plant uptake in the Iris treatment was more than four times higher for shoots than roots (p < 0.001), despite low tissue concentrations in shoots. Thus, biomass increase was more important than plant tissue concentrations in determining total plant uptake. Average TP uptake by roots was negative for both plant species (Fig. 4) because of the relatively small increase in root biomass in combination with decreased tissue concentrations. In the Iris treatment, plant uptake on average accounted for 60% (TP) and 74% (TN) of the total amount of TN and TP removed during the experiment (Table 6). In the Typha treatment, plant uptake contributed on average 49% to the total amount of TN removed and 99% to the total amount of TP removed, however, the standard deviation for TP is very high (Table 6). The difference in average percentage of plant uptake differed significantly between the Typha and Iris treatments for TN (p < 0.001) but not for TP (p = 0.650).
Fig. 3. Dry weight of Typha and Iris in the tanks at the start and end of the experiment (n = 10). Range bars show maximum and minimum values, boxes show interquartile ranges (25th–75th percentile), and black squares represent averages.
At the start of the experiment, average Typha biomass per tank (22 g) was far lower than average Iris biomass per tank (158 g), and root biomass was far larger than shoot biomass for both plant species (shoot:root biomass ratio of 0.09). After the experiment, shoot biomass was larger than root biomass in the Iris treatment with an average shoot:root biomass ratio per tank of 1.59 0.09 (SD). The shoot:root biomass ratio increased in the Typha treatment, but root biomass remained larger than shoot biomass with an average shoot:root biomass ratio per tank of 0.48 0.09 (SD) at the end of the experiment. For both plant species, average tissue concentrations of TN and TP were higher in shoots than in roots at the start of the experiment (Table 5). At the end, differences between average root and shoot tissue concentrations of TN and TP were smaller than at
Table 5 Average plant tissue concentrations ( standard deviation) of TP and TN in shoots and roots of Iris and Typha at the start and end of the experiment (n = 10). Plant species
TN (g kg Start
1
a
)
TP (g kg End
Start
a
1
) End
Iris Shoot Root
18.4 3.6 8.1 3.1
14.1 0.6 10.9 0.9
4.1 0.7 1.8 0.5
0.86 0.08 0.92 0.07
Typha Shoot Root
14.2 2.1 7.5 0.9
14.6 1.7 10.7 0.8
5.2 0.4 3.3 0.5
2.0 0.3 2.1 0.3
a Tissue concentrations at the start of the experiment are based on six individual plants, as a result, variation is higher than the variation between tanks at the end of the experiment.
Fig. 4. Estimated amount of TN (a) and TP (b) assimilated in shoot and root tissue of Iris and Typha during the experiment (n = 10). Range bars show maximum and minimum values, boxes show interquartile ranges (25th–75th percentile), and black squares represent averages. Significant differences are indicated with an asterisk (Mann–Whitney U tests, a = 0.05).
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Table 6 Total removal and estimated average plant uptake of TN and TP during the experiment (standard deviation) for the Iris and Typha treatments and plant uptake as the percentage of total removal (n = 10). Treatments indicated with different letters are significantly different (Mann–Whitney U tests, a = 0.05). Treatment
Total removal TN (g m
Iris Typha
2
25.2 0.1 2.5 0.3
)
Plant uptake TP (mg m 848 20 66 32
2
)
TN (g m
2
)
18.6 1.1a 1.2 0.3b
Percent of total removal TP (mg m
2
)
507 180a 48 37b
3.3. Floating algae
4. Discussion
Average TN (p = 0.776) and TP (p = 0.887) uptake by floating algae did not differ significantly between treatments (Fig. 5). Because of the low total TN removal from the control treatment, the average percentage of TN removal by floating algae was higher in the control than in the Iris and Typha treatments (p < 0.001 for both comparisons) (Table 7). In addition, because of low total TP removal from the control and the Typha treatment, the average percentage of TP removal by floating algae was higher in the control than in the Iris treatment (p < 0.01), and there was no significant difference between the control and the Typha treatment (p = 0.796) (Table 7).
4.1. Total removal of N and P
TN
TP
74 4a 49 12b
60 21a 99 116a
Total removal from the tanks planted with Iris was 277 mg N m 2 d 1 and 9.32 mg N m 2 d 1 during the experiment (91 days) and was significantly higher than for the Typha treatment and the control. Phosphorous removal did not differ significantly between the Typha treatment and the control while the difference in nitrogen removal was significant but small. The removal efficiencies for the FTWs planted with Iris were very high in this study (98% for TN and 92% for TP) in comparison to the removal efficiencies mentioned by Van de Moortel et al. (2010). As these authors indicated, removal efficiencies of FTWs vary considerably among studies, ranging between 6% and 83% for TP and between 25% and 40% for TN. However, comparing removal efficiency between studies in terms of percentages is difficult because these values strongly depend on the loading rate. For example, removal efficiencies for FTWs planted with Typha appear to be high for TN (57%), however, absolute nutrient removal is low due to the relatively low nutrient additions in comparison to the Iris treatment. The different treatments in our study received different amounts of nutrients during the experiment to prevent nutrient overload in any of the treatments. Nutrient concentrations in the tanks were maintained at approximately 4 mg N L 1 and 0.25 mg P L 1 comparable to ‘eutrophic surface waters’ in the Netherlands. In line with Tanner and Headley (2011), we suggest describing efficiency in terms of removal rate in milligrams (per floating mat area) per day. As indicated by Stewart et al. (2008), because of the variability among studies, the effectiveness of FTWs is hard to compare. Examples of variability in the set-up of experiments are batch vs continuous, nutrient loading, time span, the use of a control situation with or without a floating mat, the use of bottom substrates or not, and the use of soil media on the floating mat or not. All of these factors can have a large influence on experimental outcomes. In our study, the role of the sediment was deliberately excluded, because under field conditions the sediment is already present and does not add anything to removal. Especially in a system with continuous input of N and P, we wanted to focus on plant uptake and subsequent harvesting as a way of removing N and P from the system. 4.2. Plant growth and uptake
Fig. 5. Total amount of TN (a) and TP (b) assimilated in floating algae tissue per treatment (n = 10). Range bars show maximum and minimum values, boxes show interquartile ranges (25th–75th percentile), and black squares represent averages. Treatments indicated with different letters are significantly different (ANOVA, a = 0.05 for TP algae uptake and Kruskall–Wallis non-parametric test for multiple comparisons, a = 0.05 for TN algae uptake).
Of the two plant species applied in this study, only Iris showed significant results in terms of nutrient removal. In comparison to the Iris treatment, absolute TN and TP removal from the Typha treatment was negligible. The relatively low removal of TN and TP from the Typha treatment was the result of the limited increase in Typha biomass during the experiment. The average length of the Typha plants from one tank was measured on August 22, showing an average leaf height of 42 cm (based on the longest leaf) while Typha leaf height in natural stands ranges between 1 and 3 m (Grace and Harrison, 1986). Typha spp. have been widely applied in subsurface flow constructed wetlands in Europe and North America (International Water Association (IWA), 2000). FTWs
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Table 7 Total removal and average uptake by floating algae of TN and TP during the experiment (standard deviation) for all treatments and their percentage of total removal (n = 10). Treatments indicated with different letters are significantly different (Mann–Whitney U non-parametric post-hoc comparisons, Bonferroni corrected a = 0.017). Treatment
Control Iris Typha
Total removal
Floating algae uptake
Percent of total removal
TN (mg)
TP (mg)
TN (mg)
TP (mg)
TN
TP
129 79 7044 35 704 91
22 10 237 5 18 9
39.8 46.9a 33.9 14.2a 29.3 24a
4.4 4.0a 3.1 1.4a 3.8 2.7a
34 29b 0.5 0.2a 4 3a
23 24b 1 1a 20 14ab
planted with Typha have been studied by Hubbard et al. (2004) and Weragoda et al. (2012), but neither study mentioned suboptimal plant health/growth. The life cycles of Typha and Iris are similar, i.e., they are both herbaceous perennial plants that grow and bloom during spring and summer, die back every autumn/winter, and then grow again from their rootstock in spring. However, in this study it remained difficult to compare Iris and Typha directly in terms of their growth and nutrient removal capacity, because the conditions for plant growth may have varied between the two species prior to the start of the experiment. This also might explain the difference in plant biomass (22 g vs 158 g) between the two plant species at the start of the experiment. In the Iris treatment in this study, TN removal was 54 times higher than in the control treatment, and TP removal was 10 times higher (p < 0.05). On average, 74% of TN and 60% of TP removal could be explained by uptake in plant tissue. Based on this study, we conclude that plant uptake can play an important role in the removal of nitrogen and phosphorous by FTWs, but opinions in this matter vary. Kyambadde et al. (2004) drew similar conclusions based on a study showing that uptake by Cyperus papyrus was the major factor responsible for TN and TP removal; it contributed 69.5% to TN removed and 88.8% to TP removed in FTWs. For the species Miscanthidium violaceum, however, plant uptake accounted for only 15.8% of TN removed and 30.7% of TP removed. White and Cousins (2013) reported Juncus effusus accounted for 28.3% of TN removed and 41.6% of TP removed and Canna flaccida accounted for 16.4% of TN removed and 25.5% of TP removed. However, Tanner and Headley (2011) concluded that uptake of phosphorous into plant tissues could not account for more than a small fraction of the additional removal found in planted FTWs, although, FTWs planted with Cyperus ustulatus and Juncus edgariae seemed to be an exception. In accordance with Tanner and Headley (2011),Borne (2014) suggested plant uptake did not contribute significantly to the overall removal of TP from a pond retrofitted with a FTW. Our results clearly indicate Iris removed significant amounts of TN and TP from the water in the tanks during the experiment. After dividing the TP uptake rate of Iris (Table 6) by the number of days the experiment lasted (91 days) and the surface area of the floating mat (0.28 m2), we compared the resulting values with TP uptake rates for several plant species reported by Tanner and Headley (2011). The TP uptake rate of Iris of 5.57 mg P m 2 d 1 was comparable to the uptake rate for Juncus edgariae (5.2 mg P m 2 d 1) reported by Tanner and Headley (2011). However, those authors reported higher uptake rates for Cyperus ustulatus (8.5 mg P m 2 d 1) in FTWs. The TP uptake rate for Iris (0.51 g P m 2) was lower than the TP uptake rate for Canna flaccida (1.05 g P m 2) and J. effusus (1.69 g P m 2) reported by White and Cousins (2013). However, their study lasted 5 months instead of 91 days. The P uptake rates reported by Wang et al. (2014) for Pontederia cordata L. and Schoenoplectus tabernaemontani were far lower compared to our study: 1.18 mg P m 2 d 1 and 0.25 mg P m 2 d 1, respectively. A possible explanation might be the relative low concentrations of bioavailable N and P in the water described by Wang et al. (2014). The TN uptake rate of Iris (18.6 g N m 2) was comparable to the uptake rate for Canna flaccida (16.8 g P m 2) and
lower than that for J. effusus (28.5 g P m 2) reported by White and Cousins (2013). Hubbard et al. (2004) showed a far higher capacity for FTWs planted with Typha latifolia to remove nutrients from swine lagoon wastewater. The difference in phosphorous uptake between T. latifolia in their study and Iris in ours was approximately a factor of 20. This difference could not be explained by the difference in biomass increase alone, which was by a factor of 3. However, there also appeared to be a large difference in phosphorous tissue content of the plants. In the study by Hubbard et al. (2004) tissue content was on average 4.4 g P kg 1 while in our study, phosphorous tissue content dropped from 4.1 to 0.86 g P kg 1, resulting in a factor 5.1 difference. The strong decline in phosphorous tissue content we identified might be the result of lower nutrient concentrations of the water, which were never higher than 8.5 mg N L 1 and 0.7 mg P L 1, while full-strength wastewater in the study by Hubbard et al. (2004) contained on average 160 mg N L 1 and 30 mg P L 1. In accordance with our findings, Tanner and Headley (2011) also noted a strong decline in phosphorous tissue content during their experimental trials with artificial stormwater containing nutrient concentrations of 8 mg N L 1 and 0.136 mg P L 1, respectively. The results also showed that average TP uptake by roots was negative for both plant species (Fig. 4), as was also reported by Tanner and Headley (2011). The sharp decrease in TP tissue content during the experiment (in contrast to TP tissue content of the roots, TN content increased) suggests phosphorous might have been translocated from the roots to the fast(er) growing shoots. 4.3. Other processes resulting in N and P removal The higher removal of TN and TP from the Iris treatment compared to the control can only be partly explained by plant uptake (74% of TN removal and 60% of TP removal). Uptake by floating algae explained only 1% or less of TN and TP removal, leaving a large proportion unexplained. This unexplained removal could be the result of biofilm or plant-mediated processes. Stewart et al. (2008) showed that the floating mat matrix can promote a range of microbially mediated nutrient removal processes (nitrification, denitrification, and P adsorption) under controlled aeration and organic carbon additions. However, in our study, absolute amounts of TN and TP removed from the control tanks (covered with Styrofoam) were low, which suggests biofilm growth on tank walls and/or Styrofoam did not play a major role in TN and TP removal in the planted situation. Tanner and Headley (2011) drew a similar conclusion, showing that, in general, floating mats on their own (without vegetation) did not significantly enhance treatment effect. Tanner and Headley (2011) suggest that indirect effects (because artificial roots did not show benefits) of plants, such as release of bioactive compounds from the plant roots or changes in physico–chemical conditions in the water column and/or soils, might enhance sorption or sedimentation processes in the planted FTWs. However, this explanation for phosphorous removal seems less relevant in our situation, where sediment that settled to the bottom of the tanks was resuspended prior to taking
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water samples. In addition, biofilm adhered to plant roots would have been collected (for a large part) together with plant material. In the case of TN removal, reduced dissolved oxygen levels in the Iris treatment might have played an important role. Dissolved oxygen concentrations were measured continuously for 24 h in one control tank and one tank with Iris on July 19 and 20. In the control tank, dissolved oxygen concentrations never dropped below 9 mg L 1 (>100% saturation). The water in the tank with Iris was hypoxic (varied between 0.7% and 23% saturation). Kyambadde et al. (2004), Tanner and Headley (2011) and White and Cousins (2013) also found reduced dissolved oxygen concentrations beneath planted FTWs. Results from all these studies suggest that oxygen loss due to aerobic decomposition of organic matter and respiration of plant material/biofilm was the main cause of reduced dissolved oxygen concentrations beneath FTWs. The lack of oxygen in the FTWs in combination with the addition of nitrogen to the tanks primarily in the form of nitrate (ammonium:nitrate 1:20), most likely resulted in loss of nitrogen to the air due to denitrification (White and Cousins, 2013). Therefore, when applied in a field-scale trial, aeration under the FTWs might be required for the purpose of nitrification. Apart from solving problems related with excessive algae growth, FTWs could potentially play an important role in the recovery of phosphorous (Shilton et al., 2012). In situations where soil fertility is low, emergent macrophytes might by applied as a way to enhance soil fertility in the form of green manure or compost. Traore et al. (2009) showed the high potential of three aquatic invading plants (among which Typha australis) to enhance crop production in the Sahel. However, care should be taken before applying emergent macrophytes as green manure or compost. When FTWs are applied to remediate surface waters with elevated concentrations of heavy metals, macrophyte uptake and respective application as compost might lead to elevated heavy metal concentrations in crops. 5. Conclusions The results from this study suggest FTWs planted with Iris can be applied in a temperate climate to overcome problems with excessive algae growth in surface waters in urban and agricultural settings. Overall, the FTWs planted with Iris removed 277 mg N m 2 d 1 and 9.32 mg P m 2 d 1 from the water during the growing season. These values were significantly higher than the values for total removal from the control tanks, i.e., 54 times higher for TN removal and 10 times higher for TP removal. Plant uptake played a major role in the removal of nitrogen and phosphorous from the water by FTWs, i.e., 74% of TN removal and 60% of TP removal resulted from plant uptake This implies, that by harvesting plant material, phosphorous can be permanently removed from the system. Therefore, harvesting should be an integral part of FTW management practice. Based on our study there is no clear need for whole-plant harvest, because TN uptake by shoots was four times higher than root uptake and TP uptake by roots was negative. Additional research is required to study the removal efficiency of FTWs over time periods of several years. Furthermore, the possibilities for the application of harvested plant material as a marketable product should be studied.
Acknowledgements This study was funded by the Ministry of Economic Affairs (contract no. KB-14-002-036). We would like to thank Wim Dimmers, Ivo Laros, Paula Poveda, and Mario Peiró Espi for their assistance with the practical work performed during this study. References Borne, K.E., 2014. Floating treatment wetland influences on the fate and removal performance of phosphorus in stormwater retention ponds. Ecol. Eng. 69, 76– 82. Chang, N.B., Xuan, Z., Marimon, Z., Islam, K., Wanielista, M.P., 2013. Exploring hydrobiogeochemical processes of floating treatment wetlands in a subtropical stormwater wet detention pond. Ecol. Eng. 54, 66–76. De Stefani, G., Tocchetto, D., Salvato, M., Borin, M., 2011. Performance of a floating treatment wetland for in-stream water amelioration in NE Italy. Hydrobiologia 674, 157–167. Grace, J.B., Harrison, J.S., 1986. The biology of Canadian weeds. 73. Typha latifolia L., Typha angustifolia L. and Typha x glauca, Godr. Can. J. Plant Sci. 66, 361– 379. Hu, G.J., Zhou, M., Hou, H.B., Zhu, X., Zhang, W.H., 2010. An ecological floating-bed made from dredged lake sludge for purification of eutrophic water. Ecol. Eng. 36, 1448–1458. Hubbard, R.K., Gascho, G.J., Newton, G.L., 2004. Use of floating vegetation to remove nutrients from swine lagoon wastewater. Trans Am. Soc. Agric. Eng. 47 (6), 1963–1972. Hubbard, R.K., 2010. Floating vegetated mats for improving surface water quality. In: Shah, V. (Ed.), Emerging Environmental Technologies, Volume II. Springer, Netherlands, pp. 211–244. International Water Association (IWA), 2000. Constructed Wetlands for Pollution Control: Processes, Performance, Design and Operation. IWA Publishing, London. Kyambadde, J., Kansiime, F., Gumaelius, L., Dalhammar, G., 2004. A comparative study of Cyperus papyrus and Miscanthidium violaceum based constructed wetlands for wastewater treatment in a tropical climate. Water Res. 38 (2), 475– 485. Lin, Y.F., Jing, S.R., Lee, D.Y., Wang, T.W., 2002a. Nutrient removal from aquaculture wastewater using a constructed wetlands system. Aquaculture 209, 169–184. Lin, Y.F., Jing, S.R., Lee, D.Y., Wang, T.W., 2002b. Removal of solids and oxygen demand from aquaculture wastewater with a constructed wetland system in the start-up phase. Water Environ. Res. 74 (2), 136–141. Revitt, D.M., Shutes, R.B.E., Llewellyn, N.R., Worrall, P., 1997. Experimental reed bed systems for the treatment or airport runoff. Water Sci. Technol. 36 (8–9), 385– 390. Shilton, A.N., Powell, N., Guieysse, B., 2012. Plant based phosphorus recovery from wastewater via algae and macrophytes. Curr. Opin. Biotechnol. 23, 884–889. Stewart, F.M., Mulholland, T., Cunninghamm, A.B., Kania, B.G., Osterlund, M.T., 2008. Floating islands as an alternative to constructed wetlands for treatment of excess nutrients from agricultural and municipal wastes—results of laboratoryscale tests. Land Contam. Reclam. 16, 25–33. Tanner, C.C., Headley, T.R., 2011. Components of floating emergent macrophyte treatment wetlands influencing removal of stormwater pollutants. Ecol. Eng . 37, 474–486. Traore, O., Traore, K., Yaye, A., 2009. Characterization of three invading aquatic plants in Burkina Faso and their possible use for crop production. Int. J. Biol. Chem. Sci. 3 (2), 318–325. Van de Moortel, A.M.K., Meers, E., De Pauw, N., Tack, F.M.G., 2010. Effects of vegetation, season and temperature on the removal of pollutants in experimental floating treatment wetlands. Water Air Soil Pollut. 212, 281– 297. Vymazal, J., 2007. Removal of nutrients in various types of constructed wetlands. Sci. Total Environ. 380 (1–3), 48–65. Wang, C.-y., Sample, D.J., Day, S.D., Grizzard, T.J., 2014. Floating treatment wetland nutrient removal through vegetation harvest and observations from a field study. Ecol. Eng doi:http://dx.doi.org/10.1016/j.ecoleng.2014.05.018 in press. Weragoda, S.K., Jinadasa, K.B.S.N., Zhang, D.Q., Gersberg, R.M., Tan, S.K., Tanaka, N., Jern, N.W., 2012. Tropical application of floating treatment wetlands. Wetlands 32, 955–961. White, S.A., Cousins, M.W., 2013. Floating treatment wetland aided remediation of nitrogen and phosphorus from simulated stormwater runoff. Ecol. Eng. 61, 207– 215.
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Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
The contribution of plant uptake to nutrient removal by floating treatment wetlands Hanneke E. Keizer-Vlek *, Piet F.M. Verdonschot, Ralf C.M. Verdonschot, Dorine Dekkers Department of Freshwater Ecology, Alterra, Wageningen University and Research Centre, P.O. Box 47, Wageningen 6700 AA, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Received 13 March 2014 Received in revised form 4 September 2014 Accepted 26 September 2014 Available online xxx
Floating treatment wetlands (FTWs) may provide an appealing alternative to the more conventional (sub) surface flow wetlands to solve problems associated with eutrophication in urban surface waters, because they do not claim additional land area. This study examined the contribution of plant uptake to overall removal capacity of FTWs. A batch mesocosm experiment was performed during the growing season using thirty 84 L polyethylene tanks covered with 0.28 m2 floating Styrofoam mats. Ten tanks served as a control (only Styrofoam cover), 10 tanks were planted with Iris pseudacorus, and 10 with Typha angustifolia. Nutrients were added weekly to keep total nitrogen (TN) and total phosphorous (TP) concentrations at approximately 4 mg N L 1 and 0.25 mg P L 1. Total removal of TN an TP from the treatment with Typha was relatively low, resulting from the limited increase in plant biomass during the experiment. Total removal of TN and TP from the tanks planted with Iris was 277 mg N m 2 d 1 and 9.32 mg P m 2 d 1 during the experiment. These values were significantly higher than the values for total removal from the control tanks, i.e., 54 times higher for TN removal and 10 times higher for TP removal. Plant uptake played a major role in the removal of nitrogen and phosphorous from the water by FTWs, i.e., 74% of TN removal and 60% of TP removal resulted from Iris uptake. These results suggest that FTWs planted with Iris can be applied in a temperate climate to overcome problems with excessive algae growth in surface waters. ã 2014 Elsevier B.V. All rights reserved.
Keywords: Floating treatment wetland Plant biomass production Nutrient removal Eutrophication Typha angustifolia Iris pseudacorus
1. Introduction Human-induced eutrophication threatens the ecological quality of freshwater ecosystems worldwide. The problems associated with eutrophication are excessive macrophyte/algae growth resulting in oxygen depletion, stench, and fish mortality. Furthermore, the growth of toxin-excreting blue-green algae poses problems for human health. A popular way of reducing the nutrient loading to surface waters has been the construction of (sub) surface flow wetlands to treat different types of wastewater, including municipal wastewater, acid mine drainage, industrial wastewater, agricultural and storm water runoff, as well as effluent from livestock operations (Lin et al., 2002a,b,b). The advantages of (sub) surface flow constructed wetlands are moderate capital costs, very low energy consumption and maintenance requirements, and benefits of increased wildlife habitat (International
* Corresponding author. Tel.: +31 317 486423; fax: +31 317 419000. E-mail addresses: [email protected] (H.E. Keizer-Vlek), [email protected] (P.F.M. Verdonschot), [email protected] (R.C.M. Verdonschot), [email protected] (D. Dekkers). http://dx.doi.org/10.1016/j.ecoleng.2014.09.081 0925-8574/ ã 2014 Elsevier B.V. All rights reserved.
Water Association (IWA), 2000). However, these conventional wetlands are not likely to be applied in situations where land area is limited, such as in large cities. Floating treatment wetlands (FTWs) might represent a solution to the problem of limited land area because the technique does not ‘claim’ any land area. In FTWs, emergent macrophytes grow on a floating mat that is placed on the water surface. In contrast to the more conventional wetland systems, the emergent macrophytes are not anchored in the sediment of the wetland, instead, their roots hang in the water column, where the plants will take up nutrients directly. Other advantages of FTWs are their ability to cope with fluctuations in water levels, their aesthetic value (especially when using flowering plants), their provision of habitat for invertebrates, fish, and birds, and the sense of green they create in the city. Apart from FTWs, many studies have shown that free-floating aquatic plants, like water hyacinth (Eichhornia crassipes), water lettuce (Pistia stratiotes), and duckweed (Lemnaceae), can reduce nutrient concentrations in wastewater (see Hubbard, 2010, for an overview). However, because of their great colonization capacity, these species are often considered a nuisance in temperate waters, i.e., the large amounts of decomposing plant material will reduce oxygen concentrations in the
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water, resulting in fish kills and stench, they outcompete indigenous species, and large amounts of plant material will result in a diminished capacity of waterways to drain water. FTWs are being applied in various situations worldwide (Hu et al., 2010). The main applications of FTWs in terms of water quality improvement include the treatment of storm water, sewage, pond water, urban lake water, dairy manure effluent, and water supply reservoirs (Weragoda et al., 2012). A high number of studies have provided nutrient removal efficiencies for FTWs (e.g., Revitt et al., 1997; De Stefani et al., 2011; Vymazal, 2007). Different biological and physico–chemical processes play a role in nutrient removal using FTWs (e.g., nitrification, denitrification, P adsorption). However, the effect of the vegetation on overall removal performance is poorly documented (Chang et al., 2013; Van de Moortel et al., 2010). Therefore, the objective of this study was (1) to quantify the removal capacity for nitrogen and phosphorus of FTWs planted with Iris pseudacorus L. and Typha angustifolia L., respectively, and (2) to quantify the contribution of plant uptake to overall removal capacity of FTWs. 2. Methods 2.1. Experimental set-up A batch mesocosm experiment was carried out between May 30 and August 29 of 2012 in two horticultural polytunnels (5 m 8 m). Weather conditions during the experiment are presented in Table 1. Experiments were carried out in thirty 84 L polyethylene tanks with a surface opening of 0.28 m2. The tanks were placed in the tunnels according to a randomized block design (Fig. 1). Ten tanks served as a control, ten tanks were planted with Iris, and ten tanks were planted with Typha. On May 28, the tanks were filled with 70 L of groundwater from the well Nergena in Wageningen and covered with floating mats of Styrofoam 4 cm thick. After two days, the tanks were spiked with 1 mL Pokon (commercially available fertilizer for pot plants, universeel plantenvoeding, manufacturer Pokon Naturado) and 10 mL KNO3 solution. Twelve holes of approximately 2 cm 2 cm were cut in each Styrofoam cover. The next day, 100 mL water samples were collected from each tank for laboratory analysis of total nitrogen (TN) and total phosphorous (TP) in unfiltered samples by Chemisch Biologisch Laboratorium Bodem, accredited according to NEN-ENISO/IEC 17025 standard (registration number RvA L342). Prior to sampling, the biofilm attached to the walls and deposits on the bottom of the tank were brought into suspension. Additionally, two groundwater samples were collected and analyzed for TN and TP concentrations. Average nutrient concentrations in the tanks after the first nutrient additions are provided in Table 2. On June 4 and 5, 10 tanks were planted with Iris and 10 tanks were planted with Typha. The plants were supplied by Moerings B. V. in Roosendaal. The seed-raised plants were removed from their potting media by rinsing with water and placed in the tanks through holes in the Styrofoam. Each tank was planted with
Table 1 Weather conditions from May 30 to August 29 of 2012 at weather station De Deelen in the Netherlands (Source: KNMI). Variable
Value
Average temperature ( C) Average minimum temperature( C) Average maximum temperature ( C) Total rainfall (mm) Hours of sunshine Number of days without rainfall Number of days with a maximum temp of 25 C or higher
16.6 11.5 21.5 294 553 34 16
685
Fig. 1. Photo of the experimental set-up.
12 specimens of one of the two species. The Typha plants were secured to a cocktail stick pinned in the Styrofoam. From the supplied batch of plants, 12 random specimens of Iris and Typha, respectively, were kept separate to determine plant biomass (dry weight) and TN and TP tissue concentrations at the start of the experiment. NH4–N, NO2 + NO3–N, and PO4–P concentrations were monitored weekly during the experiment to avoid nutrient deficiencies in the plants arising from low nutrient concentrations in the water because of removal processes. For this purpose, a 100 mL water sample was collected weekly from a randomly selected tank of each treatment. Each week, three different tanks were sampled. Based on measured nutrient concentrations, additions of Pokon and KNO3 were made to maintain a minimum concentration of approximately 4 mg N L 1 and 0.25 mg P L 1. As a result, total nutrient additions varied depending on the treatment (Table 3). Additions with Pokon ensured the presence of trace elements (K, Fe, Mn, B, Cu, Zn, and Mo). When water levels dropped below 40 L because of evaporation and transpiration, groundwater from the well Nergena was used to top up the water level in the tanks. After 91 days, water volume in the tanks was determined. Water samples of 100 mL were collected from each tank for laboratory analysis of nutrients (TN and TP). All plants were removed from the tanks to determine plant biomass (dry weight) and TN and TP tissue concentrations at the end of the experiment. Floating algae were removed from the water surface using a small net to determine algae biomass (dry weight) and TN and TP tissue concentrations. 2.2. Plant sampling and analysis After removal of the plants from the tanks, the shoots were separated from the roots. The dry weight of roots and shoots was determined after drying to constant weight (at least 48 h) in a fancirculated oven at 70 C. The total biomass of shoots and roots was determined per tank (total of 12 plants). Representative dried tissue subsamples of roots and shoots were taken, ground, and analyzed for TN and TP by Chemisch Biologisch Laboratorium Bodem. The 12 Typha and Iris plants randomly collected at the start of the experiment received the same treatment as the plants Table 2 Average nutrient concentrations (standard deviation) in the tanks after the first nutrient additions. Treatment
TN (mg N L
Groundwater Control Iris Typha
0.09 0.04 3.85 0.28 3.90 0.11 4.07 0.42
1
)
TP (mg N L 0.02 0.02 0.15 0.02 0.17 0.02 0.17 0.01
1
)
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Table 3 Overview per treatment of the total amount of TN and TP added to each tank during the experiment. Treatment
TN (mg)
TP (mg)
Control Iris Typha
906 7217 1241
94 259 78
collected at the end of the experiment, except that dry weight and TN and TP tissue concentrations were determined for six of the 12 individual plants. Samples of floating algae were treated the same as the plant samples to determine dry weight and TN and TP tissue concentrations. 2.3. Removal capacity Average plant dry weight at the start of the experiment was calculated based on the 12 randomly selected plants of Iris and Typha. Total removal capacity was calculated by determining the total amount of nutrients added to each tank minus the amount of TN and TP present in the tank at the end of the experiment (TN and TP concentrations multiplied by the water volume). To determine plant uptake of nitrogen and phosphorous during the experiment, (estimated) dry weight at the start and end of the experiment was multiplied by TN and TP tissue concentrations at both time points. We did not correct for the addition of nutrients attributable to the addition of groundwater after evapotranspiration because this amount was negligible in comparison to the nutrient additions attributable to Pokon and KNO3. 2.4. Statistical analysis Statistical analyses were performed with IBM SPSS 19.0. In the case of TN removal and TP uptake by floating algae, data were distributed normally and variances were equal, so an ANOVA was performed. In cases of significant differences between treatments, the ANOVA was followed by post hoc testing using Tukey's HSD test. In all other cases, a non-parametric Kruskal–Wallis test for multiple comparisons was applied to test for differences between treatments because the data were not distributed normally and/or homogeneity of variance was lacking. When significant differences between treatments were present, Mann–Whitney U tests were performed. A Bonferroni correction was applied to overcome inflated Type I errors, reducing the level of significance to 0.05/ 3 = 0.017. During all other statistical tests, the level of significance was held at 0.05. 3. Results 3.1. Nitrogen and phosphorus removal Nutrient removal capacity for TP and TN differed significantly between the different treatments (p < 0.001). The removal of both TP and TN was lowest in the control and highest in the Iris treatment (Fig. 2). The difference between the control and Typha treatment was non-significant for TP (p = 0.315). TN removal capacity differed significantly between the Typha treatment and control (p < 0.001), but this difference was relatively small compared to that between the Iris treatment and control (Fig. 2). The removal efficiency for TN differed among all treatments (p < 0.001 for all comparisons). The removal efficiency was highest in the Iris treatment (98%), followed by the Typha treatment (57%) and the control (14%) (Table 4). This sequence can be explained by the fact that nutrient additions to the Typha treatment were far lower than nutrient additions to the Iris treatment (Table 3).
Fig. 2. Removal of TN (a) and TP (b) from the water in the tanks during the experiment (n = 10). Range bars show maximum and minimum values, boxes show interquartile ranges (25th–75th percentile), and black squares represent averages. Treatments indicated with different letters are significantly different (Tuckey post hoc comparisons, a = 0.5 for TN removal and Mann–Whitney U non-parametric post-hoc comparisons, Bonferroni corrected a = 0.017 for TP removal).
Although the TN removal efficiency in the Typha and Iris treatments was significantly higher than in the control treatment, the total amount of TN removed from the Typha treatment was relatively small compared to the Iris treatment (Fig. 2). The TP removal efficiency was significantly higher in the Iris treatment compared to the control and the Typha treatment (92% vs 23%, p < 0.001). There was no significant difference in TP removal efficiency between the control and the Typha treatment (p = 0.853). 3.2. Plant growth and uptake The average biomass (dry weight) of Iris increased threefold during the experiment, and the biomass of Typha doubled (Fig. 3). The increase in Iris biomass was mainly the result of an increase in shoot biomass while the Typha treatment showed an increase in both root and shoot biomass (Fig. 3). However, the absolute increase in biomass for Typha was low compared to Iris (Fig. 3). Table 4 Removal efficiency of TN and TP for the three treatments (n = 10). Treatments indicated with different letters are significantly different (Mann–Whitney U nonparametric post-hoc comparisons, Bonferroni corrected a = 0.017). Treatment
Control Iris Typha
Removal efficiency (%) TN
TP
14 9a 98 0.5b 57 7c
23 11a 92 2b 23 11a
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the start. For TN, this arose because of higher average root tissue concentrations at the end of the experiment. For TP, average tissue concentrations for both shoot and root declined during the experiment, however, average shoot concentrations declined more than average root concentrations (Table 5). Most remarkable were the very low TP concentrations in Iris for both roots and shoots at the end of the experiment. Average TN and TP plant uptake differed significantly between the Iris and Typha treatments (p < 0.001). Average TN and TP plant uptake in the Typha treatment was minimal (Fig. 4a), but average TN and TP plant uptake in the Iris treatment was more than four times higher for shoots than roots (p < 0.001), despite low tissue concentrations in shoots. Thus, biomass increase was more important than plant tissue concentrations in determining total plant uptake. Average TP uptake by roots was negative for both plant species (Fig. 4) because of the relatively small increase in root biomass in combination with decreased tissue concentrations. In the Iris treatment, plant uptake on average accounted for 60% (TP) and 74% (TN) of the total amount of TN and TP removed during the experiment (Table 6). In the Typha treatment, plant uptake contributed on average 49% to the total amount of TN removed and 99% to the total amount of TP removed, however, the standard deviation for TP is very high (Table 6). The difference in average percentage of plant uptake differed significantly between the Typha and Iris treatments for TN (p < 0.001) but not for TP (p = 0.650).
Fig. 3. Dry weight of Typha and Iris in the tanks at the start and end of the experiment (n = 10). Range bars show maximum and minimum values, boxes show interquartile ranges (25th–75th percentile), and black squares represent averages.
At the start of the experiment, average Typha biomass per tank (22 g) was far lower than average Iris biomass per tank (158 g), and root biomass was far larger than shoot biomass for both plant species (shoot:root biomass ratio of 0.09). After the experiment, shoot biomass was larger than root biomass in the Iris treatment with an average shoot:root biomass ratio per tank of 1.59 0.09 (SD). The shoot:root biomass ratio increased in the Typha treatment, but root biomass remained larger than shoot biomass with an average shoot:root biomass ratio per tank of 0.48 0.09 (SD) at the end of the experiment. For both plant species, average tissue concentrations of TN and TP were higher in shoots than in roots at the start of the experiment (Table 5). At the end, differences between average root and shoot tissue concentrations of TN and TP were smaller than at
Table 5 Average plant tissue concentrations ( standard deviation) of TP and TN in shoots and roots of Iris and Typha at the start and end of the experiment (n = 10). Plant species
TN (g kg Start
1
a
)
TP (g kg End
Start
a
1
) End
Iris Shoot Root
18.4 3.6 8.1 3.1
14.1 0.6 10.9 0.9
4.1 0.7 1.8 0.5
0.86 0.08 0.92 0.07
Typha Shoot Root
14.2 2.1 7.5 0.9
14.6 1.7 10.7 0.8
5.2 0.4 3.3 0.5
2.0 0.3 2.1 0.3
a Tissue concentrations at the start of the experiment are based on six individual plants, as a result, variation is higher than the variation between tanks at the end of the experiment.
Fig. 4. Estimated amount of TN (a) and TP (b) assimilated in shoot and root tissue of Iris and Typha during the experiment (n = 10). Range bars show maximum and minimum values, boxes show interquartile ranges (25th–75th percentile), and black squares represent averages. Significant differences are indicated with an asterisk (Mann–Whitney U tests, a = 0.05).
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Table 6 Total removal and estimated average plant uptake of TN and TP during the experiment (standard deviation) for the Iris and Typha treatments and plant uptake as the percentage of total removal (n = 10). Treatments indicated with different letters are significantly different (Mann–Whitney U tests, a = 0.05). Treatment
Total removal TN (g m
Iris Typha
2
25.2 0.1 2.5 0.3
)
Plant uptake TP (mg m 848 20 66 32
2
)
TN (g m
2
)
18.6 1.1a 1.2 0.3b
Percent of total removal TP (mg m
2
)
507 180a 48 37b
3.3. Floating algae
4. Discussion
Average TN (p = 0.776) and TP (p = 0.887) uptake by floating algae did not differ significantly between treatments (Fig. 5). Because of the low total TN removal from the control treatment, the average percentage of TN removal by floating algae was higher in the control than in the Iris and Typha treatments (p < 0.001 for both comparisons) (Table 7). In addition, because of low total TP removal from the control and the Typha treatment, the average percentage of TP removal by floating algae was higher in the control than in the Iris treatment (p < 0.01), and there was no significant difference between the control and the Typha treatment (p = 0.796) (Table 7).
4.1. Total removal of N and P
TN
TP
74 4a 49 12b
60 21a 99 116a
Total removal from the tanks planted with Iris was 277 mg N m 2 d 1 and 9.32 mg N m 2 d 1 during the experiment (91 days) and was significantly higher than for the Typha treatment and the control. Phosphorous removal did not differ significantly between the Typha treatment and the control while the difference in nitrogen removal was significant but small. The removal efficiencies for the FTWs planted with Iris were very high in this study (98% for TN and 92% for TP) in comparison to the removal efficiencies mentioned by Van de Moortel et al. (2010). As these authors indicated, removal efficiencies of FTWs vary considerably among studies, ranging between 6% and 83% for TP and between 25% and 40% for TN. However, comparing removal efficiency between studies in terms of percentages is difficult because these values strongly depend on the loading rate. For example, removal efficiencies for FTWs planted with Typha appear to be high for TN (57%), however, absolute nutrient removal is low due to the relatively low nutrient additions in comparison to the Iris treatment. The different treatments in our study received different amounts of nutrients during the experiment to prevent nutrient overload in any of the treatments. Nutrient concentrations in the tanks were maintained at approximately 4 mg N L 1 and 0.25 mg P L 1 comparable to ‘eutrophic surface waters’ in the Netherlands. In line with Tanner and Headley (2011), we suggest describing efficiency in terms of removal rate in milligrams (per floating mat area) per day. As indicated by Stewart et al. (2008), because of the variability among studies, the effectiveness of FTWs is hard to compare. Examples of variability in the set-up of experiments are batch vs continuous, nutrient loading, time span, the use of a control situation with or without a floating mat, the use of bottom substrates or not, and the use of soil media on the floating mat or not. All of these factors can have a large influence on experimental outcomes. In our study, the role of the sediment was deliberately excluded, because under field conditions the sediment is already present and does not add anything to removal. Especially in a system with continuous input of N and P, we wanted to focus on plant uptake and subsequent harvesting as a way of removing N and P from the system. 4.2. Plant growth and uptake
Fig. 5. Total amount of TN (a) and TP (b) assimilated in floating algae tissue per treatment (n = 10). Range bars show maximum and minimum values, boxes show interquartile ranges (25th–75th percentile), and black squares represent averages. Treatments indicated with different letters are significantly different (ANOVA, a = 0.05 for TP algae uptake and Kruskall–Wallis non-parametric test for multiple comparisons, a = 0.05 for TN algae uptake).
Of the two plant species applied in this study, only Iris showed significant results in terms of nutrient removal. In comparison to the Iris treatment, absolute TN and TP removal from the Typha treatment was negligible. The relatively low removal of TN and TP from the Typha treatment was the result of the limited increase in Typha biomass during the experiment. The average length of the Typha plants from one tank was measured on August 22, showing an average leaf height of 42 cm (based on the longest leaf) while Typha leaf height in natural stands ranges between 1 and 3 m (Grace and Harrison, 1986). Typha spp. have been widely applied in subsurface flow constructed wetlands in Europe and North America (International Water Association (IWA), 2000). FTWs
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Table 7 Total removal and average uptake by floating algae of TN and TP during the experiment (standard deviation) for all treatments and their percentage of total removal (n = 10). Treatments indicated with different letters are significantly different (Mann–Whitney U non-parametric post-hoc comparisons, Bonferroni corrected a = 0.017). Treatment
Control Iris Typha
Total removal
Floating algae uptake
Percent of total removal
TN (mg)
TP (mg)
TN (mg)
TP (mg)
TN
TP
129 79 7044 35 704 91
22 10 237 5 18 9
39.8 46.9a 33.9 14.2a 29.3 24a
4.4 4.0a 3.1 1.4a 3.8 2.7a
34 29b 0.5 0.2a 4 3a
23 24b 1 1a 20 14ab
planted with Typha have been studied by Hubbard et al. (2004) and Weragoda et al. (2012), but neither study mentioned suboptimal plant health/growth. The life cycles of Typha and Iris are similar, i.e., they are both herbaceous perennial plants that grow and bloom during spring and summer, die back every autumn/winter, and then grow again from their rootstock in spring. However, in this study it remained difficult to compare Iris and Typha directly in terms of their growth and nutrient removal capacity, because the conditions for plant growth may have varied between the two species prior to the start of the experiment. This also might explain the difference in plant biomass (22 g vs 158 g) between the two plant species at the start of the experiment. In the Iris treatment in this study, TN removal was 54 times higher than in the control treatment, and TP removal was 10 times higher (p < 0.05). On average, 74% of TN and 60% of TP removal could be explained by uptake in plant tissue. Based on this study, we conclude that plant uptake can play an important role in the removal of nitrogen and phosphorous by FTWs, but opinions in this matter vary. Kyambadde et al. (2004) drew similar conclusions based on a study showing that uptake by Cyperus papyrus was the major factor responsible for TN and TP removal; it contributed 69.5% to TN removed and 88.8% to TP removed in FTWs. For the species Miscanthidium violaceum, however, plant uptake accounted for only 15.8% of TN removed and 30.7% of TP removed. White and Cousins (2013) reported Juncus effusus accounted for 28.3% of TN removed and 41.6% of TP removed and Canna flaccida accounted for 16.4% of TN removed and 25.5% of TP removed. However, Tanner and Headley (2011) concluded that uptake of phosphorous into plant tissues could not account for more than a small fraction of the additional removal found in planted FTWs, although, FTWs planted with Cyperus ustulatus and Juncus edgariae seemed to be an exception. In accordance with Tanner and Headley (2011),Borne (2014) suggested plant uptake did not contribute significantly to the overall removal of TP from a pond retrofitted with a FTW. Our results clearly indicate Iris removed significant amounts of TN and TP from the water in the tanks during the experiment. After dividing the TP uptake rate of Iris (Table 6) by the number of days the experiment lasted (91 days) and the surface area of the floating mat (0.28 m2), we compared the resulting values with TP uptake rates for several plant species reported by Tanner and Headley (2011). The TP uptake rate of Iris of 5.57 mg P m 2 d 1 was comparable to the uptake rate for Juncus edgariae (5.2 mg P m 2 d 1) reported by Tanner and Headley (2011). However, those authors reported higher uptake rates for Cyperus ustulatus (8.5 mg P m 2 d 1) in FTWs. The TP uptake rate for Iris (0.51 g P m 2) was lower than the TP uptake rate for Canna flaccida (1.05 g P m 2) and J. effusus (1.69 g P m 2) reported by White and Cousins (2013). However, their study lasted 5 months instead of 91 days. The P uptake rates reported by Wang et al. (2014) for Pontederia cordata L. and Schoenoplectus tabernaemontani were far lower compared to our study: 1.18 mg P m 2 d 1 and 0.25 mg P m 2 d 1, respectively. A possible explanation might be the relative low concentrations of bioavailable N and P in the water described by Wang et al. (2014). The TN uptake rate of Iris (18.6 g N m 2) was comparable to the uptake rate for Canna flaccida (16.8 g P m 2) and
lower than that for J. effusus (28.5 g P m 2) reported by White and Cousins (2013). Hubbard et al. (2004) showed a far higher capacity for FTWs planted with Typha latifolia to remove nutrients from swine lagoon wastewater. The difference in phosphorous uptake between T. latifolia in their study and Iris in ours was approximately a factor of 20. This difference could not be explained by the difference in biomass increase alone, which was by a factor of 3. However, there also appeared to be a large difference in phosphorous tissue content of the plants. In the study by Hubbard et al. (2004) tissue content was on average 4.4 g P kg 1 while in our study, phosphorous tissue content dropped from 4.1 to 0.86 g P kg 1, resulting in a factor 5.1 difference. The strong decline in phosphorous tissue content we identified might be the result of lower nutrient concentrations of the water, which were never higher than 8.5 mg N L 1 and 0.7 mg P L 1, while full-strength wastewater in the study by Hubbard et al. (2004) contained on average 160 mg N L 1 and 30 mg P L 1. In accordance with our findings, Tanner and Headley (2011) also noted a strong decline in phosphorous tissue content during their experimental trials with artificial stormwater containing nutrient concentrations of 8 mg N L 1 and 0.136 mg P L 1, respectively. The results also showed that average TP uptake by roots was negative for both plant species (Fig. 4), as was also reported by Tanner and Headley (2011). The sharp decrease in TP tissue content during the experiment (in contrast to TP tissue content of the roots, TN content increased) suggests phosphorous might have been translocated from the roots to the fast(er) growing shoots. 4.3. Other processes resulting in N and P removal The higher removal of TN and TP from the Iris treatment compared to the control can only be partly explained by plant uptake (74% of TN removal and 60% of TP removal). Uptake by floating algae explained only 1% or less of TN and TP removal, leaving a large proportion unexplained. This unexplained removal could be the result of biofilm or plant-mediated processes. Stewart et al. (2008) showed that the floating mat matrix can promote a range of microbially mediated nutrient removal processes (nitrification, denitrification, and P adsorption) under controlled aeration and organic carbon additions. However, in our study, absolute amounts of TN and TP removed from the control tanks (covered with Styrofoam) were low, which suggests biofilm growth on tank walls and/or Styrofoam did not play a major role in TN and TP removal in the planted situation. Tanner and Headley (2011) drew a similar conclusion, showing that, in general, floating mats on their own (without vegetation) did not significantly enhance treatment effect. Tanner and Headley (2011) suggest that indirect effects (because artificial roots did not show benefits) of plants, such as release of bioactive compounds from the plant roots or changes in physico–chemical conditions in the water column and/or soils, might enhance sorption or sedimentation processes in the planted FTWs. However, this explanation for phosphorous removal seems less relevant in our situation, where sediment that settled to the bottom of the tanks was resuspended prior to taking
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water samples. In addition, biofilm adhered to plant roots would have been collected (for a large part) together with plant material. In the case of TN removal, reduced dissolved oxygen levels in the Iris treatment might have played an important role. Dissolved oxygen concentrations were measured continuously for 24 h in one control tank and one tank with Iris on July 19 and 20. In the control tank, dissolved oxygen concentrations never dropped below 9 mg L 1 (>100% saturation). The water in the tank with Iris was hypoxic (varied between 0.7% and 23% saturation). Kyambadde et al. (2004), Tanner and Headley (2011) and White and Cousins (2013) also found reduced dissolved oxygen concentrations beneath planted FTWs. Results from all these studies suggest that oxygen loss due to aerobic decomposition of organic matter and respiration of plant material/biofilm was the main cause of reduced dissolved oxygen concentrations beneath FTWs. The lack of oxygen in the FTWs in combination with the addition of nitrogen to the tanks primarily in the form of nitrate (ammonium:nitrate 1:20), most likely resulted in loss of nitrogen to the air due to denitrification (White and Cousins, 2013). Therefore, when applied in a field-scale trial, aeration under the FTWs might be required for the purpose of nitrification. Apart from solving problems related with excessive algae growth, FTWs could potentially play an important role in the recovery of phosphorous (Shilton et al., 2012). In situations where soil fertility is low, emergent macrophytes might by applied as a way to enhance soil fertility in the form of green manure or compost. Traore et al. (2009) showed the high potential of three aquatic invading plants (among which Typha australis) to enhance crop production in the Sahel. However, care should be taken before applying emergent macrophytes as green manure or compost. When FTWs are applied to remediate surface waters with elevated concentrations of heavy metals, macrophyte uptake and respective application as compost might lead to elevated heavy metal concentrations in crops. 5. Conclusions The results from this study suggest FTWs planted with Iris can be applied in a temperate climate to overcome problems with excessive algae growth in surface waters in urban and agricultural settings. Overall, the FTWs planted with Iris removed 277 mg N m 2 d 1 and 9.32 mg P m 2 d 1 from the water during the growing season. These values were significantly higher than the values for total removal from the control tanks, i.e., 54 times higher for TN removal and 10 times higher for TP removal. Plant uptake played a major role in the removal of nitrogen and phosphorous from the water by FTWs, i.e., 74% of TN removal and 60% of TP removal resulted from plant uptake This implies, that by harvesting plant material, phosphorous can be permanently removed from the system. Therefore, harvesting should be an integral part of FTW management practice. Based on our study there is no clear need for whole-plant harvest, because TN uptake by shoots was four times higher than root uptake and TP uptake by roots was negative. Additional research is required to study the removal efficiency of FTWs over time periods of several years. Furthermore, the possibilities for the application of harvested plant material as a marketable product should be studied.
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