Article pubs.acs.org/est
Ecological Engineering Approaches to Improve Hydraulic Properties of Infiltration Basins Designed for Groundwater Recharge Morgane Gette-Bouvarot, Laurence Volatier, Laurent Lassabatere, Damien Lemoine, Laurent Simon, Cécile Delolme, and Florian Mermillod-Blondin* UMR 5023 LEHNA, Université de Lyon, CNRS, Université Claude Bernard Lyon 1, ENTPE, 6 rue Raphaël Dubois, 69622 Villeurbanne, France S Supporting Information *
ABSTRACT: Infiltration systems are increasingly used in urban areas for groundwater recharge. The reduction of sediment permeability by physical and/or biological processes is a major problem in management of infiltration systems often requiring expensive engineering operations for hydraulic performance maintenance. To reduce these costs and for the sake of sustainable development, we proposed to evaluate the ability of ecological engineering approaches to reduce the biological clogging of infiltration basins. A 36-day field-scale experiment using enclosures was performed to test the influences of abiotic (light reduction by shading) and biotic (introduction of the macrophyte Vallisneria spiralis (L.) or the gastropod Viviparus viviparus (Linnaeus, 1758)) treatments to limit benthic biofilm biomass and to maintain or even increase hydraulic performances. We coupled biological characterization of sediment (algal biomass, bacterial abundance, total organic carbon, total nitrogen, microbial enzymatic activity, photosynthetic activity, and photosystem II efficiency) with hydraulic conductivity measurements to assess the effects of treatments on sediment permeability. The grazer Viviparus viviparus significantly reduced benthic biofilm biomass and enhanced hydraulic conductivity. The other treatments did not produce significant changes in hydraulic conductivity although Vallisneria spiralis affected photosynthetic activity of biofilm. Finally, our results obtained with Viviparus viviparus are promising for the development of ecological engineering solutions to prevent biological fouling in infiltration systems.
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systems8 and specific solutions have to be applied depending on the clogging processes (biological and/or physicochemical) involved. The technical treatment regularly applied for recovery of the hydraulic performance of infiltration basins involves the removal of the top sediment layer of lowest permeability.3,8 Such management techniques are energy- and resourceintensive operations such as the scraping, transport for disposal and/or reuse of removed sediments and the cost for the purchase and the implementation of a new calibrated sediment layer, that is, an overall cost of approximately 255,000 € for an infiltration basin of 10 000 m2 receiving streamwater (data obtained from Veolia Water and Greater Lyon Urban Community). In parallel, increased interest in sustainability has resulted in approaches integrating ecology and engineering into a formal application.14−16 The resulting field called “ecological engineering” combines basic and applied science for the restoration, design, and construction of ecosystems.17−19 We expect that application of ecological engineering
INTRODUCTION Half of the world’s population lives in cities and this number is predicted to reach 60% in 2030.1 Many cities are groundwater dependent and it is estimated that 2 billion people in the world rely on groundwater for drinking-water supply.2 Facing the needs of abundant and safe resources of groundwater, managed aquifer recharge (MAR) systems have been developed to augment groundwater resources.3,4 MAR practices like aquifer storage and recovery (ASR), soil aquifer treatment (SAT) or riverbank filtration (RBF) are diversified and received waters of different qualities such as streamwater, stormwater, or treated wastewater.5,6 Despite this diversity of practices, one of the principal areas of concern in these engineered systems is the clogging of the infiltration medium that could impair their hydraulic performances.3,6−8 Indeed, infiltration systems are commonly built using sand as an infiltration medium for water purification purpose,9 but the small particle size of sand favors the retention of suspended particles and offers a high specific area available for biofilm establishment.8 Consequently, sandy infiltration media are progressively subject to clogging by the combined and overlapping processes of pore occlusion by fine particles and excessive biofilm growth7,10−13 but also by chemical precipitations.8 Therefore, the maintenance of sediment permeability is a major operational issue for MAR © 2015 American Chemical Society
Received: Revised: Accepted: Published: 9936
April 1, 2015 July 23, 2015 July 27, 2015 July 27, 2015 DOI: 10.1021/acs.est.5b01642 Environ. Sci. Technol. 2015, 49, 9936−9944
Article
Environmental Science & Technology approaches could be efficient to prevent the clogging and/or restore the hydraulic performance of infiltration systems designed for MAR with streamwater. Thus, our intention in the present study was to search for an ecological process to maintain/increase hydraulic conductivity of infiltration basins used for groundwater recharge. In a previous study,13 we pointed out that the saturated hydraulic conductivity of the infiltration basins was mainly controlled by the phototrophs of benthic biofilms (i.e., diatoms, green algae, and cyanobacteria) rather than by physical (sedimentation of fine particles) or chemical (calcium carbonate precipitation) processes. Consequently, we especially searched for treatments able to regulate algal biofilm growth at the water/sediment interface and, consequently, improve the hydraulic performance of infiltration basins. The phototrophic biofilm growth is controlled by abiotic factors such as light and nutrient availabilities.20−23 Then, competitive interactions for these factors may exist with other phototrophs, such as phytoplankton and aquatic macrophytes, and may regulate algal growth at the water− sediment interface.24 Ecological interactions among phototrophs also concern allelopathic processes associated with the release of chemical compounds by an organism that can inhibit the growth or the development of neighboring organisms by affecting their structure and/or their activity.25,26 Allelopathic macrophytes may therefore be of prime interest to control algal biofilm at the water-sediment interface.27 Manipulations of food webs like top predator introductions in lakes have been recognized to affect all trophic levels in the ecosystem (topdown control17,28,29). Similarly, the grazing pressure of invertebrates on benthic biofilms may be an efficient way to significantly reduce algal growth at the water-sediment interface.30−32 Based on these basic ecological principles, we tested three different ecological conditions (reduction of light, introduction of a macrophyte, introduction of a grazing invertebrate) on benthic biofilm and associated hydraulic conductivity using in situ enclosures in an infiltration basin. Four treatments were applied during 5 weeks: (1) enclosures with reduction of light intensity by shading,33 (2) enclosures with addition of the macrophyte Vallisneria spiralis (L.) which could reduce algal biofilm by allelopathy,27 (3) enclosures with addition of the gastropod Viviparus viviparus (Linnaeus, 1758) which was recognized as an efficient algal grazer,34,35 and (4) enclosures acting as controls (without addition of macro-organisms or shading). Measurements of hydraulic conductivity were coupled with analyses on the sediment structure including the mineral part (grain size distribution) and the benthic biofilm (algal biomass, bacterial abundance, total organic carbon, total nitrogen, photosynthetic activity and efficiency, hydrolytic activity) at the start and the end of the experiment. This coupling was crucial to evaluate, for the first time, the ability of ecological engineering solutions to maintain/increase infiltration basin performances through biological interactions.
Figure 1. Photography of the water-sediment interface colonized by algal biofilms (a), scheme of an experimental unit (b), photography of the experimental units in the basin (c), and photography of an experimental unit with individuals of Viviparus viviparus (d).
hydraulic conductivities (Ks < 10−5 m.s−1). This basin has not been subject to drying for 1 month preceding the experiment and the water supply has been maintained to ensure a water column varying from 1.0 to 1.8 m according to the usual monitoring of the basins.13 Assessments of the benthic fauna at the start and the end of the experiment in all enclosures showed that nematodes and oligochaetes were the dominant taxa in the basin with abundances of 7370 and 2200 individuals.m−2, respectively. We also measured lower densities of several grazer species: the gastropod Limnea stagnalis (390 individuals.m−2) and ephemera from the group of Baetidae (165 individuals.m−2). A correspondence analysis made with the data set of benthic invertebrates (excluding added Viviparus viviparus) showed comparable benthic community structure for the four treatments at the end of the experiment (Figure S1, Supporting Information). We also weekly measured in situ temperature, conductivity, pH, and dissolved oxygen (DO) concentrations in the water column during the course of the experiment (36 days) to characterize the physico-chemistry of infiltrated water. These measurements were performed with HQ40D multiparameter probe (HACH). Mean (±standard deviations) of temperature, conductivity, pH and DO were 15 ± 3 °C, 299 ± 39 μS.cm−1, 8.8 ± 0.3, and 13 ± 7 mg·L−1, respectively. Nutrient concentrations were also weekly measured and obtained from filtered water (0.7 μm) conserved at 4 °C before analysis within 24 h with a sequential analyzer using colorimetric methods.13 As in previous experiments,13,27 oligotrophic conditions were found in the basin with concentrations of NO3−, NH4+, PO43−, and dissolved organic carbon (DOC) of 338 ± 71 μg·L−1, 16.7 ± 15.2 μg·L−1, 12.6 ± 3.7 μg·L−1, 4.05 ± 1.08 mg·L−1, respectively. Experimental Units. Enclosures consisted of stainless steel cylinders (internal diameter of 30 cm, height of 14 cm) firmly buried into the sediment at a depth of 11 cm (Figure 1b). The top of the each cylinder was set at 3 cm above the sediment surface to limit experimental artifacts (edge effects) and to allow water exchange between the interior and the exterior of the enclosures. Twelve enclosures were manually and carefully placed 1 week before the start of the experiment in the center of the infiltration basin to prevent bank effects (Figure 1c). Nets with a mesh size of 0.5 cm were fixed at the top of all enclosures because of the potential escape of gastropods during the course of the experiment (Figure 1d). The “shading” treatment was achieved by covering the enclosures with stainless steel disks drilled with holes of 0.05 mm enabling water exchanges between the inside and the outside of the
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MATERIALS AND METHODS Study Site. The experiment was set up in the “CrépieuxCharmy” pumping well field (375 ha, 1 280 000 inhabitants supplied) near Lyon (France). Twelve infiltration basins are used on this site for aquifer recharge with surface water pumped from a channel (Vieux Rhône) of the Rhone River. Basins were usually scraped every 3 years to restore their hydraulic performances. We selected a basin characterized by a dense algal biofilm (Figure 1a) and zones with reduced saturated 9937
DOI: 10.1021/acs.est.5b01642 Environ. Sci. Technol. 2015, 49, 9936−9944
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made with a cut syringe was done for evaluating the physiological state of the algal biofilm (net photosynthetic activity and efficiency of the photosystem II). Sampling was conducted just after the hydraulic measurements, with water in the basin, to prevent any drying and disturbance of sediment and biofilm. All samples were then stored in a cool box during transport to the laboratory within 4 h. Hydraulic Conductivity Measured in Enclosures. Insitu infiltration measurements were performed in each enclosure under saturated conditions at the start and the end of the experiment before sediment and biofilm samplings. Measurements were done according to the “falling head method”.39−41 The method consists in inserting a tube into the ground, applying an initial water head into the tube and following the drop of water head with time. The diameter of the Plexiglas standpipe was 5 cm, the initial water heads were about 70−80 cm and five tests were performed per enclosure. During a test, the time required for the water in the standpipe to drop from the upper to the lower levels was recorded every centimeter. From each test, we obtained an infiltration curve representing the temporal evolution of water head with time. As initial water head conditions have an influence on the temporal evolution of water head (h), we used the following normalization calculation:
enclosures. Previous measurements made in the laboratory under variable light intensities showed that this “shading” treatment reduced by 80% the light intensity reaching the sediment surface. Macro-Organisms Studied. The macrophyte Vallisneria spiralis was selected according to a previous experiment showing its significant effect on algal biofilms.27 We chose the gastropod Viviparus viviparus because it efficiently feeds on algal biofilms35 and its gill breathing allows it to be encaged underwater. Moreover, the two selected species are not exotic species in the Rhone river floodplain and then can be introduced in the “Crépieux-Charmy” pumping well field which is a NATURA 2000 area. Specimens of Vallisneria spiralis (length of leaves ∼10 cm) and Viviparus viviparus (size of shells ∼2 cm) were collected in a cut off channel of the Rhône River located at less than 1 km from the infiltration basin. Both macrophytes and animals were acclimated in aquariums filled with sediment and water from the basin for 15 days before the start of the experiment. For the two species, we used natural densities observed in aquatic systems: 100 individuals.m−2 for Viviparus viviparus (see Jakubik36 for densities in various freshwater habitats) and 60 individuals.m−2 for Vallisneria spiralis (see Bornette et al.37 for densities in cut off channels of the Rhône River). Such density of Vallisneria spiralis resulted in a low plant cover ( 0.1 for all tested effects). Therefore, despite a significant reduction of algal biomass in treatments with Viviparus viviparus, microbial activity involved in organic matter degradation and net photosynthetic activity (Figure 4b) were not affected by gastropod grazing. These results highlight the fact that grazing stimulated the biofilm activity per unit of biomass (i.e., photosynthetic activity reported per Chla concentration). 9941
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basins. Our experimental approach, based on in situ enclosures, clearly showed that the grazing activity of the gastropod Viviparus viviparus was very efficient to reduce algal biomass and to prevent the effect of clogging on hydraulic conductivities. Moreover, the gastropod treatment did not affect the microbial activities involved in organic matter processing (hydrolytic activity), highlighting the efficiency of this treatment for both the hydraulic and the self-purification performances of the basin. Although the present experiment was limited in time (5 weeks), we are confident on the longterm performance of such ecological treatment because Viviparus viviparus presents biological traits (trophic habits, reproductive traits,35) allowing the maintenance of populations regardless the seasonal dynamics of algal biomass (lowest in winter). Now, experiments are needed to validate the long-term viability of Viviparus viviparus introduction for the maintenance of hydraulic performance of infiltration basins. In contrast with this trophic (top-down) control of benthic algal biomass by gastropods, the treatments based on light limitation (shading) or allelopathic macrophytes did not significantly affect algal biomass and hydraulic conductivity during our 5-week long experiment. It is probable that a significant influence of these treatments on algal growth could be obtained during longer experiments but the resulting influence of these treatments on hydraulic conductivity is more prone to discussion. Finally, the present study is the first to highlight the potentiality of ecological engineering approach for management of MAR systems supplied with streamwater. It is worth to note that the same ecological treatments should not be efficient in MAR systems receiving wastewater and urban waters that are highly concentrated with fine mineral and organic particles. In these systems, other ecological engineering approaches need to be developed to prevent clogging. For example, use of aquatic tubificid worms that can produce dense gallery networks in MAR basins clogged by fine particles supplied with stormwater could be an efficient way to increase hydraulic performances.60,61 For MAR systems supplied with streamwater and clogged by algal biofilms, our results are very promising and the gastropod Viviparus viviparus seems an excellent actor for limiting clogging. Based on these results, we aim to develop basin-scale tests to evaluate the viability of Viviparus viviparus on the long-term by considering the seasonal dynamics of this species but also those of the biofilm during several years.
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Figure 4. Assessments of (a) maximal efficiency of photosystem II, (b) photosynthetic activity, and (c) hydrolytic activity of the biofilm measured at t0 and tf in enclosures for the four treatments (mean ± standard deviation, n = 3 per treatment). Significant differences between t0 and tf for a treatment (Tukey’s HSD tests) are indicated with stars on bar charts.
ASSOCIATED CONTENT
* Supporting Information S
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.5b01642. Results concerning the sediment grain size analyses and benthic fauna in the basin are available in Table S1 and Figure S1, respectively (PDF)
This stimulating effect could be due to three mechanisms: (1) the removal of senescent cells and detritic organic matter increasing light penetration and nutrient availability for remaining and new cells,56,57 (2) a nutrient enrichment by excretion,58,59 and (3) increased hydraulic conductivity due to grazing (Figure 2) which enhanced the nutrient supply to biofilm colonizing the top sediment layer. Further experiments are needed to decrypt mechanisms involved in the stimulating effect of grazing on biofilm activities. Implications for the Management of Infiltration Basins. In the present study, we tested three “ecological engineering” treatments to limit and/or reduce algal biomass accrual which affects the hydraulic performance of infiltration
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AUTHOR INFORMATION
Corresponding Author
*Phone: +33 4 72 43 13 64; fax: +33 4 72 04 77 43; e-mail: fl
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank all people involved in the measurements of Ks in the field and analyses performed in the laboratory. So, many thanks 9942
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(17) Mitsch, W. Ecological engineering: a cooperative role with the planetary life-support system. Environ. Sci. Technol. 1993, 27 (3), 438− 445. (18) Mitsch, W. J. What is ecological engineering? Ecol. Eng. 2012, 45, 5−12. (19) Mitsch, W. J.; Jørgensen, S. E. Ecological Engineering and Ecosystem Restoration; John Wiley & Sons: New York, 2004. (20) Stevenson, J. R., Bothwell, M. L., Lowe, R. L., Eds. Algal Ecology: Freshwater Benthic Ecosystems; Academic Press: London, 1996. (21) Bourassa, N.; Cattaneo, A. Control of periphyton biomass in Laurentian streams (Quebec). J. North Am. Benthol. Soc. 1998, 17 (4), 420−429. (22) Armitage, A. R.; Gonzalez, V. L.; Fong, P. Decoupling of nutrient and grazer impacts on a benthic estuarine diatom assemblage. Estuarine, Coastal Shelf Sci. 2009, 84 (3), 375−382. (23) Sturt, M. M.; Jansen, M. A. K.; Harrison, S. S. C. Invertebrate grazing and riparian shade as controllers of nuisance algae in a eutrophic river. Freshwater Biol. 2011, 56 (12), 2580−2593. (24) Sand-Jensen, K.; Borum, J. Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquat. Bot. 1991, 41 (1−3), 137−175. (25) Van Donk, E.; Van de Bund, W. J. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquat. Bot. 2002, 72 (3−4), 261−274. (26) Gross, E. M. Allelopathy of aquatic autotrophs. Crit. Rev. Plant Sci. 2003, 22 (3−4), 313−339. (27) Gette-Bouvarot, M.; Mermillod-Blondin, F.; Lemoine, D.; Delolme, C.; Etienne, L.; Volatier, L. The potential of allelopathic macrophytes to control benthic biofilm growth − a mesocosm approach. Ecol. Eng. 2015, 75, 178−186. (28) Carpenter, S. R.; Kitchell, J. F.; Hodgson, J. R.; Cochran, P. A.; Elser, J. J.; Elser, M. M.; Lodge, D. M.; Kretchmer, D.; He, X.; von Ende, C. N. Regulation of lake primary productivity by food web structure. Ecology 1987, 68, 1863−1876. (29) Brett, M. T.; Goldman, C. R. A meta-analysis of the freshwater trophic cascade. Proc. Natl. Acad. Sci. U. S. A. 1996, 93 (15), 7723− 7726. (30) Feminella, J. W.; Hawkins, C. P. Interactions between stream herbivores and periphyton: A quantitative analysis of past experiments. J. North Am. Benthol. Soc. 1995, 14 (4), 465−509. (31) Steinman, A. D. Effects of grazers on freshwater benthic algae. In Algal Ecology; Stevenson, R. J., Bothwell, M. L., Lowe, R. L., Eds.; Academic Press: London, 1996; pp 343−373. (32) Haglund, A. L.; Hillebrand, H. The effect of grazing and nutrient supply on periphyton associated bacteria. FEMS Microbiol. Ecol. 2005, 52 (1), 31−41. (33) Stevenson, R. J. Resource thresholds and stream ecosystem sustainability. J. North Am. Benthol. Soc. 1997, 16 (2), 410−424. (34) Liess, A.; Kahlert, M. Gastropod grazers and nutrients, but not light, interact in determining periphytic algal diversity. Oecologia 2007, 152 (1), 101−111. (35) Jakubik, B. Food and feeding of Viviparus viviparus (L.) (Gastropoda) in dam reservoir and river habitats. Polym. J. Ecol. 2009, 57 (2), 321−330. (36) Jakubik, B. Life strategies of Viviparidae (Gastropoda: Caenogastropoda: Architaenioglossa) in various aquatic habitats: Viviparus viviparus (Linnaeus, 1758) and V. contectus (Millet, 1813). Folia Malacol. 2012, 20 (3), 145−179. (37) Bornette, G.; Piegay, H.; Citterio, A.; Amoros, C.; Godreau, V. Aquatic plant diversity in four river floodplains: a comparison at two hierarchical levels. Biodivers. Conserv. 2001, 10, 1683−1701. (38) Lamberti, G. A. Grazing experiments in artificial streams. In Research in Artificial Streamsapplications, Uses, And Abuses; Lamberti, G. A., Steinman, A. D., Eds.; J. North Am. Benthol. Soc., 1993, 12: 337−342. (39) Rodgers, M.; Mulqueen, J. Field-saturated hydraulic conductivity of unsaturated soils from falling-head well tests. Agr. Water Manag. 2006, 79, 160−176.
to Alexandre Elaphos, Thérèse Bastide, Alicia Naveros, Margot Jacquy, Felix Vallier, Jean-Philippe Bedell, Dieuseul Predelus, Artur Coutinho, Marouen Shabou, Chantal Mora, and Marc Danjean. This research was done on the Research Platform of Crépieux-Charmy (Plate-forme de recherche de CrépieuxCharmy) and received financial and technical support from the Lyon Metropole and Veolia Water. We also thank three anonymous referees for advice and constructive comments on the manuscript.
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REFERENCES
(1) United Nations. Department of Economic and Social Affairs, Population Division, 2007. World Population Prospects: The 2012 revision, highlights and Advance Tables, Working paper No. ESA/P/ WP.228; United Nations: New York, 2013; http://esa.un.org/wpp/ Documentation/pdf/WPP2012_HIGHLIGHTS.pdf. (2) Morris, B. L.; Lawrence, A. R. L.; Chilton, P. J. C.; Adams, B.; Calow, R. C.; Klinck, B. A. Groundwater and Its Susceptibility to Degradation: A Global Assessment of the Problem and Options for Management, Early warning and assessment report series, RS 03-3; United Nations Environment Programme: Nairobi, 2003 (3) Bouwer, H. Artificial recharge of groundwater: Hydrogeology and engineering. Hydrogeol. J. 2002, 10 (1), 121−142. (4) Hunt, W. F.; Traver, R. G.; Davis, A. P.; Emerson, C. H.; Collins, K. A.; Stagge, J. H. Low impact development practices: designing to infiltrate in urban environments. In Effects of Urbanization on Groundwater: An Engineering Case-Based Approach for Sustainable Development; Chang, N. B., Ed.; American Society of Civil Engineers: Reston, VA, 2010; pp 308−346. (5) Dillon, P. Future management of aquifer recharge. Hydrogeol. J. 2005, 13 (1), 313−316. (6) Martin, R., Ed. Clogging Issues Associated with Managed Aquifer Recharge Methods; IAH Commission on Managing Aquifer Recharge: Australia, 2013. (7) Baveye, P.; Vandevivere, P.; Hoyle, B. L.; DeLeo, P. C.; de Lozada, D. S. Environmental impact and mechanisms of the biological clogging of saturated soils and aquifer materials. Crit. Rev. Environ. Sci. Technol. 1998, 28 (2), 123−191. (8) Knowles, P.; Dotro, G.; Nivala, J.; García, J. Clogging in subsurface-flow treatment wetlands: Occurrence and contributing factors. Ecol. Eng. 2011, 37 (2), 99−112. (9) Dodds, W. K.; Randel, C. A.; Edler, C. C. Microcosms for aquifer research: application to colonization of various sized particles by ground-water microorganisms. Groundwater 1996, 34 (4), 756−759. (10) Platzer, C.; Mauch, K. Soil clogging in vertical flow reed beds mechanisms, parameters, consequences and.......solutions? Water Sci. Technol. 1997, 35 (5), 175−181. (11) Langergraber, G.; Haberl, R.; Laber, J.; Pressl, A. Evaluation of substrate clogging processes in vertical flow constructed wetlands. Water Sci. Technol. 2003, 48 (5), 25−34. (12) Thullner, M.; Zeyer, J.; Kinzelbach, W. Influence of microbial growth on hydraulic properties of pore networks. Transp. Porous Media 2002, 49 (1), 99−122. (13) Gette-Bouvarot, M.; Mermillod-Blondin, F.; Angulo-Jaramillo, R.; Delolme, C.; Lemoine, D.; Lassabatere, L.; Loizeau, S.; Volatier, L. Coupling hydraulic and biological measurements highlights the key influence of algal biofilm on infiltration basin performance. Ecohydrology 2014, 7 (3), 950−964. (14) Mitsch, W. J., Jørgensen, S. E., Eds. Ecological Engineering: An Introduction to Ecotechnology; Wiley: New York, 1989. (15) Byers, J. E.; Cuddington, K.; Jones, C. G.; Talley, T. S.; Hastings, A.; Lambrinos, J. G.; Crooks, J. A.; Wilson, W. G. Using ecosystem engineers to restore ecological systems. Trends Ecol. Evol. 2006, 21 (9), 493−500. (16) Bakshi, B. R.; Ziv, G.; Lepech, M. D. Techno-ecological synergy: a framework for sustainable engineering. Environ. Sci. Technol. 2015, 49 (3), 1752−1760. 9943
DOI: 10.1021/acs.est.5b01642 Environ. Sci. Technol. 2015, 49, 9936−9944
Article
Environmental Science & Technology
(60) Nogaro, G.; Mermillod-Blondin, F.; François-Carcaillet, F.; Gaudet, J. P.; Lafont, M.; Gibert, J. Invertebrate bioturbation can reduce the clogging of sediment: an experimental study using filtration sediment columns. Freshwater Biol. 2006, 51, 1458−1473. (61) Nogaro, G.; Mermillod-Blondin, F. Stormwater sediment and bioturbation influences on hydraulic functioning, biogeochemical processes, and pollutant dynamics in laboratory infiltration systems. Environ. Sci. Technol. 2009, 43, 3632−3638.
(40) Pedescoll, A.; Uggetti, E.; Llorens, E.; Granés, F.; García, D.; García, J. Practical method based on saturated hydraulic conductivity used to assess clogging in subsurface flow constructed wetlands. Ecol. Eng. 2009, 35, 1216−1224. (41) Pedescoll, A.; Samsó, R.; Romero, E.; Puigagut, J.; García, J. Reliability, repeatability and accuracy of the falling head method for hydraulic conductivity measurements under laboratory conditions. Ecol. Eng. 2011, 37, 754−757. (42) Blott, S. J.; Pye, K. GRADISTAT: a grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth Surf. Processes Landforms 2001, 26 (11), 1237−1248. (43) Unesco. Determination of Photosynthetic Pigments in Seawater. Monographs on Oceanographic Methodology; Imprimerie Rolland: Paris, France, 1966. (44) Mermillod-Blondin, F.; Winiarski, T.; Foulquier, A.; Perrissin, A.; Marmonier, P. Links between sediment structures and ecological processes in the hyporheic zone: ground penetrating radar as a noninvasive tool to detect subsurface biologically-active zones. Ecohydrology 2015, 8, 626−641. (45) Mermillod-Blondin, F.; Gaudet, J.-P.; Gerino, M.; Desrosiers, G.; Jose, J.; Creuzé des Châtelliers, M. Relative influence of bioturbation and predation on organic matter processing in river sediments: a microcosm experiment. Freshwater Biol. 2004, 49, 895− 912. (46) Navel, S.; Mermillod-Blondin, F.; Montuelle, B.; Chauvet, E.; Simon, L.; Piscart, C.; Marmonier, P. Interactions between fauna and sediment characteristics control plant matter breakdown in river sediments. Freshwater Biol. 2010, 55, 753−766. (47) Maxwell, K.; Johnson, G. N. Chlorophyll fluorescence - a practical guide. J. Exp. Bot. 2000, 51 (345), 659−668. (48) Ibaraki, Y.; Murakami, J. Distribution of chlorophyll fluorescence parameter Fv/Fm within individual plants under various stress conditions. Acta Hort. 2007, 761, 255−260. (49) Mauclaire, L.; Schürmann, A.; Thullner, M.; Gammeter, S.; Zeyer, J. Sand filtration in a water treatment plant: Biological parameters responsible for clogging. J. Water Supply: Res. Technol. AQUA 2004, 53 (2), 93−108. (50) Cuker, B. E. Grazing and nutrient interactions in controlling the activity and composition of the epilithic algal community of an arctic lake. Limnol. Oceanogr. 1983, 28 (1), 133−141. (51) Hillebrand, H. Meta-analysis of grazer control of periphyton biomass across aquatic ecosystems. J. Phycol. 2009, 45 (4), 798−806. (52) Rober, A. R.; Wyatt, K. H.; Stevenson, R. J. Regulation of algal structure and function by nutrients and grazing in a boreal wetland. J. North Am. Benthol. Soc. 2011, 30 (3), 787−796. (53) Xian, Q.; Chen, H.; Liu, H.; Zou, H.; Yin, D. Isolation and identification of antialgal compounds from the leaves of Vallisneria spiralis L. by activity-guided fractionation. Environ. Sci. Pollut. Res. 2006, 13, 233−237. (54) Leu, E.; Krieger-Liszkay, A.; Goussias, C.; Gross, E. M. Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum inhibit photosystem II. Plant Physiol. 2002, 130, 2011− 2018. (55) Zhu, J.; Liu, B.; Wang, J.; Gao, Y.; Wu, Z. Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte (Myriophyllum spicatum) and its secretion. Aquat. Toxicol. 2010, 98, 196−203. (56) McCormick, P. V.; Stevenson, R. J. Grazer control of nutrient availability in the periphyton. Oecologia 1991, 86 (2), 287−291. (57) Skov, M. W.; Volkelt-Igoe, M.; Hawkins, S. J.; Jesus, B.; Thompson, R. C.; Doncaster, C. P. Past and present grazing boosts the photo-autotrophic biomass of biofilms. Mar. Ecol. Prog. Ser. 2010, 401, 101−111. (58) Kahlert, M.; Baunsgaard, M. T. Nutrient recycling: a strategy of a grazer community to overcome nutrient limitation. J. North Am. Benthol. Soc. 1999, 18 (3), 363−369. (59) Arakelova, E. S. Periphyton grazing and phosphorus excretion by mollusks. Russ. J. Ecol. 2010, 41 (4), 327−332. 9944
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