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a CH2M HILL, 555 South Flower Street, Suite 3550, Los Angeles, CA 90071
b Dep. of Land Resources and Environmental Sciences, Montana State Univ., P.O. Box 173120, Bozeman, MT 59717-3120
c Dep. of Civil Engineering and Center for Biofilm Engineering, Montana State Univ., P.O. Box 173900, Bozeman, MT 59717-3900
* Corresponding author (wallen{at}ch2m.com)
Received for publication March 29, 2001.
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ABSTRACT |
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 TOPNOTES ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Abbreviations: COD, chemical oxygen demand • DO, dissolved oxygen • DOC, dissolved organic carbon • OM, organic matter • SSW, subsurface-flow wetland
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INTRODUCTION |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Reviews of operational data for full-scale systems indicate that SSWs can meet effluent criteria in cold climates, and that temperature effects on removal of organic matter (OM) may be less than expected (Kadlec and Knight, 1996; USEPA, 2000). The lack of significant temperature effects on OM removal in full-scale SSWs has been attributed to sedimentation, temperature adaptation of microbes, variation in decomposition rates, and thermal buffering by plant litter, snow, and ground heat, but mechanistic explanations remain speculative (Kadlec and Knight, 1996; Wittgren and Maehlum, 1997). It is also possible that seasonal differences in oxygen release from plant roots may contribute to the lack of temperature response; however, the relative contribution of plant oxygen transport to wastewater treatment remains controversial. Some wetland designers assume that plant oxygen transport is significant (e.g., Campbell and Ogden, 1999; DeBusk and DeBusk, 2001), while others dismiss it as negligible compared with oxygen demand and undependable due to seasonal senescence (USEPA, 2000).
Wetland plants are known to transport oxygen into their roots to support aerobic respiration and to oxidize phytotoxic reduced compounds (Fe2+, Mn2+, S2-) in the rhizosphere. Some wetland plants can release enough oxygen into the root zone to support aerobic microbial activity (Reddy et al., 1989b; Bodelier et al., 1996; Armstrong et al., 1990), and this may sometimes represent as much as 90% of the total oxygen entering a wetland substrate (Reddy et al., 1989a). Quantification of oxygen flux from entire root systems has been complicated by species and seasonal differences, spatial heterogeneity, and other measurement issues such as oxygen demand of the root zone solution and root to solution volume (Bedford et al., 1991; Sorrell and Armstrong, 1994). Plants' capacity to supply oxygen to the root zone varies among species due to differences in vascular tissues, metabolism, and root distribution (Gersberg et al., 1986; Steinberg and Coonrod, 1994; Jackson and Armstrong, 1999). Because root and rhizome respiration consumes most oxygen that diffuses through plant shoots and oxygen demand for root and rhizome respiration declines with temperature, the potential for plants to release oxygen into the root zone may increase during cold periods (Howes and Teal, 1994; Callaway and King, 1996).
Based on the temperature and species effects on oxygen release reported in the ecological literature, we hypothesized that (i) plants would modify the effects of temperature on root zone oxidation and wastewater treatment in SSWs and (ii) plant effects on temperature responses would vary among species. We tested these hypotheses in a relatively long-term (28-mo) greenhouse experiment using batch incubations in subsurface-flow wetland microcosms at temperatures from 4 to 24°C. In this paper, we contrast results for incubations at the maximum and minimum temperatures (August 1998 and January 1999), which illustrate major differences between the growing season and winter.
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MATERIALS AND METHODS |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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A synthetic wastewater simulating secondary domestic effluent was mixed from sucrose, hydrolyzed meat protein, and inorganic nutrient and metal salts to ensure consistent, known composition for all incubations (Allen, 1999). Mean influent concentrations of the main constituents were measured to be 151 mg organic C L-1 (chemical oxygen demand [COD] = 470 mg L-1), 44 mg N L-1 (27 mg amino N L-1 [TN persulfate digestion; 0–150 mg L-1 test, Hach Company, Loveland, CO], 17 mg NH4–N L-1 [modified Berthelot method]), 8 mg PO4–P L-1 (Dionex [Sunnyvale, CA] Model DX-500), and 14 mg SO4–S L-1. Columns were gravity-drained and filled with fresh, synthetic wastewater 3 d before each incubation, and then again at the start of each incubation. Dilution of the influent wastewater attributed to water retained in the porous media was determined to be 
5% using a bromide tracer, and showed no significant difference among plant treatments.
Calculations were made to determine the significance of dissolved oxygen (DO) inputs associated with water added to replace evaporative losses. Evaporative losses were greater for planted columns than for unplanted controls, but did not vary among species. The maximum evapotranspiration (ET) rate for planted columns at 24°C was measured to be 0.7 L d-1 column-1. Assuming an oxygen solubility of 8.5 mg O2 L-1, this corresponded to an input of approximately 6 mg O2 d-1 column-1 or 1% of the influent COD per day. The maximum ET rate for planted columns at 4°C was less than 0.4 L d-1 column-1. Assuming an oxygen solubility of 13 mg O2 L-1, this corresponded to an input of less than 5 mg O2 d-1 column-1 or 1% of the influent COD per day.
Column solution samples were collected with a 60-mL syringe after three sampling tube volumes (approximately 25 mL) had been withdrawn and discarded. Solution samples collected from 5-, 15-, and 30-cm depths during preliminary incubations showed no measurable vertical gradients for COD, dissolved organic carbon (DOC), or SO2-4. Samples were subsequently collected from 15 cm only. Samples were collected from four replicates immediately after filling columns and on Days 1, 3, 6, 9, 14, and 20 of each incubation. Samples were analyzed immediately for chemical oxygen demand (COD; 0–1500 mg L-1 test; Hach Company), then filtered to sterilize (0.22-µm cellulose acetate filter), stored in sterile test tubes at 2°C, and analyzed for SO2-4 using ion chromatography (Dionex Model DX-500). Two replicates were also sampled (i) every 4 h for the first 16 h, (ii) at 32 and 48 h, and (iii) on Days 3, 6, 9, 14, and 20 for additional dissolved organic carbon (DOC) analyses. These samples were filtered (0.20-µm nylon filter), acidified with 20% H3PO4, and analyzed using a Dohrmann DC-80 carbon analyzer (Xertex Corp., Santa Clara, CA).
Two flow-through cells, one housing a standard O2 electrode (Yellow Springs Instruments [Yellow Springs, OH] Model 5739) and the other a flat-surface pH electrode, were operated in series to measure DO and pH when collecting samples for COD, DOC, and SO2-4 analyses. As described above, one solution sample was collected using a 60-mL syringe. After aliquots for laboratory analyses were removed, approximately 10 pore volumes (40 mL) of the original solution sample were passed through the flow cells and DO and pH readings were recorded. The DO and pH probes were checked against reference solutions before and after sampling.
Platinum redox electrodes (Faulkner et al., 1989) were permanently installed in all 32 columns at 5-, 15-, and 30-cm depths, connected to a computer via a multiplexer, and read automatically every 4 h. Columns were connected by a salt bridge with two saturated calomel reference electrodes located centrally (Veneman and Pickering, 1983). Redox potential (Eh) was estimated from measured electrode potential by adding 244 mV (Stumm and Morgan, 1996). Because pH was consistently circumneutral (average 6.8 with and 7.0 without plants) and the effect of temperature on measured potential is relatively small (Stumm and Morgan, 1996), Eh was not corrected for pH or temperature. Redox probes were checked periodically against a ferrous–ferric standard solution (Light, 1972).
Data were analyzed by repeated measures analysis of variance, with time and depth (for Eh) as within-subjects factors. Data for both temperatures and all incubation times, plant treatments, and depths were first analyzed together. Because statistical interactions among factors were common, separate analyses were then performed for different temperatures, times, treatments, or depths as needed to clarify results. Analyses were conducted using SAS Version 6.12 (SAS Institute, 1996). All differences reported below were statistically significant at p = 0.05. There were four replicates for COD, SO2-4, DO, and pH, and two for DOC. There were eight replicates for Eh normally, but only five for cattail and controls in August 1998.
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RESULTS |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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At both temperatures, COD and DOC removal was initially rapid, slowed over time, and asymptotically approached a relatively persistent residual level. Temperature and plant effects developed rapidly after the start of incubations. After 4 h at 24°C, DOC removal averaged 40% for all treatments; at 4°C, 4-h removal averaged 41% for controls and cattail but 58% for sedge and bulrush, though only sedge and controls differed significantly. After 24 h at 24°C, COD removal averaged 52% and DOC removal averaged 59%, with no significant differences among treatments. At 4°C, COD removal over 24 h was significantly less in control and cattail columns (55%) than in sedge and bulrush columns (80%); DOC removal was significantly lower in controls (50%) than sedge and bulrush columns (80%).
The greater COD removal for sedge and bulrush at 4°C generally continued throughout time within each incubation. Differences were greatest on Days 3 and 6 and then diminished somewhat (Fig. 3). Final COD removal was relatively complete for sedge and bulrush at both temperatures (93–96%). At 24°C final COD removal for cattail and controls was also relatively complete (89 and 81%, respectively). However, at 4°C final removal was 77% for cattail columns and 67% for unplanted controls.
The two indicators of root zone oxidation status, Eh and SO2-4 concentration, were affected significantly by plant treatment, temperature, and incubation time, and Eh sometimes varied significantly with depth (Fig. 4). Patterns of Eh and SO2-4 concentration were consistent with those for COD and DOC removal: plant effects on Eh and SO2-4 were greater at low temperatures, and sedge and bulrush enhanced root zone oxidation. Dissolved oxygen was consistently below 1 mg L-1 and did not vary with temperature or plant treatment.
Averaged across all depths and times at 4°C, Eh values were significantly higher in sedge and bulrush columns than in cattail and control columns (Fig. 4). In contrast, when averaged across all depths and times at 24°C, Eh did not differ significantly among treatments. At 24°C, Eh values were higher in sedge and bulrush columns than cattail and control columns at the 5-cm depth, but not at 15 or 30 cm. In sedge and bulrush columns, Eh was higher at 4 than 24°C at all depths, but in cattail and control columns, Eh remained low at both temperatures.
Redox potentials and sulfate concentrations were high immediately after filling the columns with fresh wastewater and generally decreased rapidly within 24 h (Fig. 4). At 4°C and all depths, Eh decreased from an initial range of approximately +250 to +450 mV to a range of approximately -170 to +40 mV within 24 h. In cattail and control columns, Eh reached a minimum of approximately -220 to -170 mV by Day 3 and remained near this level for the rest of the incubation. In contrast, Eh in sedge and bulrush columns reached a minimum of approximately -200 to +20 mV by Day 3, but values increased continuously after Days 3 to 6 and reached final values of approximately +140 to +430 mV, which were approximately 340 to 640 mV greater than in controls. As depth increased, minimum Eh values in sedge and bulrush columns decreased and persisted longer, and the final values decreased. Plant species effects on Eh at 4°C were significant except during the time period 8 to 48 h.
Plant species and depth effects on Eh were far less pronounced at 24°C (Fig. 4). No plant effects were observed at 15 and 30 cm, and values were approximately -230 to -130 mV from Day 1 through Day 20. At 5 cm, however, plant species effects were similar to those observed at 4°C, but weaker. Again, Eh approached minimum values in 1 d in all columns, but in bulrush and sedge columns Eh values increased after 3 to 6 d, while values remained low in cattail and control columns. Unlike at 4°C, the increase was more pronounced in bulrush than sedge.
As with COD, DOC, and Eh, plant effects on sulfate concentration were more pronounced at low temperature (Fig. 4). Across all times at 4°C, plant species influenced SO2-4 concentrations significantly, with higher values in sedge and bulrush columns than in cattail and control columns. At 24°C, SO2-4 concentrations were uniformly low and were not influenced significantly by plants. Sulfate concentrations in sedge and bulrush columns were higher at 4 than 24°C, but temperature did not affect SO2-4 concentrations in cattail and control columns.
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DISCUSSION |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Greater dissolved OM removal and increased root zone oxidation for sedge and bulrush columns at low temperature were potentially due to both an increase in oxygen flux from plant roots and a decrease in root zone decomposition processes that produce dissolved OM, but the absence of this temperature response in cattail and control columns suggests that oxygen flux from sedge and bulrush root systems was significant. Our indirect indicators of root zone oxygen supply, Eh and SO2-4 in the bulk solution, represent the net effect of plants and microbes on root zone oxidation status, and should not be confused with measurements of actual oxygen flux from roots (Bedford et al., 1991; Steinberg and Coonrod, 1994; Jespersen et al., 1998). Nonetheless, other studies have suggested greater potential for plants to supply oxygen for root zone processes at low than high temperatures (Gries et al., 1990; Howes and Teal, 1994; Callaway and King, 1996). Oxygen consumption by root respiration, which varies seasonally with temperature and plant growth, appears to be the major variable influencing root zone oxygen supply (Howes and Teal, 1994). In our study, plant effects on Eh and SO2-4 concentrations generally developed when oxygen consumption by plants and microbes was probably lowest; that is, at low temperature, as described above, or in later days of 24°C incubations, after most dissolved OM had been consumed. Studying a reed bed system, Griffin et al. (1999) reported indirect evidence for seasonal differences in root zone oxidation; sulfide odor was a problem during summer but not during winter at low temperatures. Sulfate is converted to sulfide by sulfate-reducing bacteria only after oxygen and other more thermodynamically favorable electron acceptors have been depleted.
We interpret the relationships among changes in COD, Eh, and SO2-4 during low-temperature incubations as reflecting a strong connection between total oxygen demand and root zone oxidation status (Fig. 5) . For all planted and unplanted columns, the majority of COD removal at 4°C occurred within 24 h and was associated with a rapid reduction in Eh values and SO2-4 concentrations. However, removal of COD was more rapid in sedge and bulrush columns than in cattail and control columns even though the associated decreases in Eh values and SO2-4 concentrations were less pronounced, suggesting greater oxygen supply to the bulk solution, presumably due to oxygen flux from plant roots. In cattail and control columns, COD depletion slowed after 24 h and Eh values and SO2-4 concentrations remained low, indicating there was insufficient oxygen supply to meet all respiratory demands. In sedge and bulrush columns, COD was largely depleted after 3 to 6 d; thereafter, Eh values rose steadily. Sulfate concentrations began to rise after Day 9, indicating that oxygen supply may have exceeded respiratory demands and was sufficient for some sulfide oxidation. Similar to other findings that measurement of oxidation around root tips is influenced by the reducing capacity of the soil (Flessa and Fischer, 1992), there appeared to be a threshold of low dissolved OM (in this case COD equal to approximately 30 mg L-1 for sedge and bulrush) that had to be reached before oxygen flux from plant roots could be expressed as an increase in Eh of the bulk solution. This threshold was reached in sedge and bulrush columns at 4°C and to a more limited extent at 24°C, but it was not reached in cattail columns. Seasonal patterns of OM removal, Eh, and SO2-4 over the entire study period were consistent with these interpretations (Hook et al., 2002).
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Our results, together with evidence from field studies (Kadlec and Knight, 1996; Smith et al., 1997; Wittgren and Maehlum, 1997) and recent research on arctic and alpine soil microbiology (Brooks et al., 1996; Schmidt et al., 1999), reinforce doubts about two common assumptions in SSW design: (i) that biological treatment processes are insignificant at temperatures near freezing, and (ii) that plants have a minimal role in treatment processes. There is substantial evidence that even at temperatures near and below 0°C soil microbial processes can be significant and regulated by factors other than temperature, such as organic matter quantity and quality, electron acceptor availability, or nutrient availability (Brooks et al., 1996; Schmidt et al., 1999). In operational SSWs, water temperatures often remain above freezing even when air temperatures are well below 0°C for long periods (Kadlec and Knight, 1996; Smith et al., 1997). Our microcosm results suggest that effective organic matter removal in SSWs is possible at temperatures near freezing, depending on the presence and species of plants. Somewhat surprisingly, differences in OM removal and root zone oxidation among species were greatest at low temperatures, suggesting a key role for plants especially during dormancy.
Reviews that question the importance of plant selection to SSW performance (USEPA, 2000) may reflect emphasis on continuous high organic matter loading and warm temperatures in comparative studies, as well as the greater complexity and lack of statistical replication in operational treatment wetlands. The controlled environments used here were not intended to recreate realistic winter conditions of operational SSWs, and the relatively small size of our experimental units may have accentuated root and shoot density and, therefore, altered plant effects. Nonetheless, our experiments represented a wide range of temperatures and OM levels (due to depletion over time within incubations), achieved a degree of control and replication not feasible in the field, and allowed for careful evaluation of the relative performance of species tested. The success, especially in winter, of sedge, which is much less researched than bulrush or cattail, points to the need to investigate additional plant species and to quantify the role of oxygen flux from root systems in operational cold-climate SSWs.
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ACKNOWLEDGMENTS |
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NOTES |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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REFERENCES |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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