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a USDA–ARS, George E. Brown Jr. Salinity Lab., 450 W. Big Springs Rd., Riverside, CA 92507-4617
b USDA–ARS, Environmental Microbial Safety Lab., Bldg. 173, Rm. 203, BARC–East Power Mill Rd., Beltsville, MD 20705
* Corresponding author (sbradford{at}ussl.ars.usda.gov)
Received for publication June 7, 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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Abbreviations: CAFO, concentrated animal feeding operation • CSD, cumulative size distribution • DOM, dissolved organic matter • EC, electrical conductivity • MSE, mean square error • PV, pore volume
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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Hancock et al. (1998) indicated that Giardia were sometimes present in ground water, especially in infiltration galleries and horizontal wells. Consistent with this finding, 6% of the ground water–associated disease outbreaks in the USA from 1971 to 1996 have been attributed to Giardia (USEPA, 2000). This information has important implications for treatment techniques of surface water or effluent from sewage treatment plants that rely on soil passage to remove cysts (i.e., riverbank filtration, infiltration basins and trenches, and sand filters). It also implies that ground water under the direct influence of surface water may be vulnerable to contamination by Giardia. Hence, knowledge of the processes and factors that control the transport and deposition of cysts in soils is needed to protect drinking water supplies.
Considerable research has been devoted to the transport and fate of bacteria and viruses in porous media (reviews are given by Schijven and Hassanizadeh, 2000; Harvey and Harms, 2002; Jin and Flury, 2002; Ginn et al., 2002; de Jonge et al., 2004). Cysts of Giardia are much larger (8–12 µm) than most of these waterborne pathogens (<2 µm). Because of their relatively large size, Giardia are typically assumed to have limited transport potential and little research has therefore examined their transport in porous media (Swertfeger et al., 1999; Hsu et al., 2001). Several studies have, however, examined the transport and deposition behavior of Cryptosporidium oocysts (Mawdsley et al., 1996a, 1996b; Brush et al., 1999; Swertfeger et al., 1999; Harter et al., 2000; Hsu et al., 2001; Logan et al., 2001; Tufenkji et al., 2004; Bradford and Bettahar, 2005; Tufenkji and Elimelech, 2005). Cryptosporidium parvum is also a pathogenic protozoan parasite, but is smaller in size (3–6 µm) than Giardia. Results from these studies suggests that deposition of Cryptosporidium oocysts in porous media will depend on a specific combination of physical (grain size and surface roughness, pore water velocity, and preferential flow pathways) and chemical (oocyst chemical properties, grain surface charge, and solution pH and ionic strength) properties of a given system.
Attachment, mechanical filtration, and straining are potential mechanisms for colloid (cysts of Giardia) deposition that have been identified (McDowell-Boyer et al., 1986). Attachment involves collision with and fixation to the porous medium, and depends on colloid–colloid, colloid–solvent, and colloid–porous media interactions (Elimelech and O'Melia, 1990). Clean-bed attachment behavior is traditionally described as a first-order process and the spatial distribution of retained colloids will hence assume an exponential shape (e.g., Tufenkji et al., 2003). Mechanical filtration refers to the complete retention of colloids at the soil surface because the colloids are larger than the soil pores (McDowell-Boyer et al., 1986). Straining involves the entrapment of colloids in down-gradient pores and at grain junctions that are too small to allow particle passage, and consequently increases with increasing size of the colloid and decreasing sand size (Bradford et al., 2003). In contrast to mechanical filtration, straining only happens in the smaller portions of the pore space and transport of colloids can still occur in the pore networks that are larger than the colloid diameter. Straining is most pronounced at the soil surface or at the boundary of different soil textures where colloids are encountering a new pore network (Bradford et al., 2002, 2003, 2004, 2005). At such boundaries, colloids are more likely to encounter a pore smaller than the critical straining size or a pore larger than the critical size that steers colloids toward "dead-end regions" of the pore space. Once colloids have entered the hydraulically active network, size exclusion and advection make it more likely for the colloids to be transported within the network because it is formed by relatively large pores. Water permeability functions of sandy soils (e.g., van Genuchten et al., 1991) show that most of the saturated flow in sands occurs in large pores that are substantially larger than colloid sizes.
Although pathogens are of fecal origin, most transport experiments have been conducted in the absence of dissolved manure suspensions. Manure suspensions consist of a complex mixture of partially digested organic matter and microbial biomass, and therefore encompasses a wide range in particle sizes. Pathogens constitute only a small portion of the colloid-sized particles in this suspension. The subsurface transport of pathogens such as Giardia are likely to be influenced by the presence of this complex mixture. For example, straining and/or mechanical filtration of larger manure particles could decrease the effective size of the pores or fill and/or block smaller pore spaces completely. The potential implications of such manure deposition on pathogen transport are not yet known, and no published studies have examined the transport behavior of manure suspensions in conjunction with pathogen transport. Manure deposition induced changes in the soil pore sizes could also promote pathogen retention via straining, or induce changes in the pore-scale water flow field that would confine pathogens to more conductive (larger and less reactive) regions of the pore space.
Published research using dissolved organic matter (DOM) such as humic and fulvic acids suggests that manure suspensions may also influence the attachment behavior of pathogens. For example, DOM has been reported to enhanced microbe transport (Johnson and Logan, 1996; Pieper et al., 1997; Powelson and Mills, 2001). Blocking of favorable attachment sites by organic matter has typically been used to explain this enhanced transport (Johnson and Logan, 1996; Pieper et al., 1997). Dissolved organic matter has also been reported to sorb onto bacterial cell walls and alter their electrophoretic mobility (Gerritson and Bradley, 1987). Increasing the negative charge of the bacterial surface diminishes its attachment onto negatively charged solid surfaces (Sharma et al., 1985). Other researchers have reported that organic matter inhibits microbe transport due to hydrophobic interactions between microbe and grain surfaces that are coated with organic matter (Bales et al., 1993; Kinoshita et al., 1993). Adsorption of pathogens onto mobile manure colloids could also facilitate their transport potential (Jin et al., 2000; de Jonge et al., 2004).
This study examines the transport of manure suspensions and cysts of Giardia in several sands. Special attention was given to mechanisms of manure particle and Giardia deposition, and the influence of manure suspensions on cyst migration. Effluent concentration curves, deposition data, temporal changes in the manure effluent size distribution, and numerical modeling were used to quantify mechanisms controlling the transport and deposition of manure particles and Giardia in several sands. To help identify the role of manure suspension on Giardia transport, migration behavior in the presence and absence of manure suspensions was compared.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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Manure Suspension
Dairy calf manure was collected under the crates of 1- to 12-wk-old calves, thoroughly mixed with a stick, and then stored at 4°C. The manure suspension was prepared by mixing a known mass of this manure (wet wt.) with the 0.001 M NaBr solution. This suspension was then filtered through a 103-µm stainless steel wire mesh. The concentrated suspension was then diluted to achieve a concentration of approximately 4.0 g L–1 (mass based on unfiltered weight). The pH and EC of the filtered manure suspension were 8.8 and 0.38 dS m–1, respectively. The optical density at 660 nm was measured on liquid samples containing manure suspension using an Unico UV-2000 spectrophotometer (United Products & Instruments, Dayton, NJ). The manure suspension concentration was determined from a linear calibration curve between standard manure suspensions and optical density readings. Particle-size distribution information for selected liquid samples containing manure suspension were determined using a Horiba LA 930 laser scattering particle size analyzer (Horiba Instruments, Irvine, CA).
Cysts of Giardia
Cysts of Giardia range in size from 8 to 12 µm in diameter, and their density is around 1.04 g cm–3 (Medema et al., 1998). The electrophoretic mobility of the Giardia lamblia cysts obtained from Waterborne (New Orleans, LA) was measured to be –0.88 µm s–1 V–1 cm (corresponding to a zeta potential of –12 mV) in the 0.001 M NaBr solution using a ZetaPALs instrument (Brookhaven Instruments Corp., Holtsville, NY).
The concentrations of Giardia in liquid samples were determined using the protocol described by Bradford and Schijven (2002). In brief, 0.5 mL of concentrated (10x) PST solution was added to 4 mL of the aqueous sample to facilitate the release of cysts and to minimize sorption losses. The PST (1x) solution consists of phosphate buffered saline solution containing 2% (mass/volume) sodium dodecyl sulfate, and 2% (v/v) Tween 80. This solution was gently mixed and then centrifuged for 10 min at 1150 x g. The supernatant was pipetted down to 300 µL and the pellet was resuspended. Cysts were subsequently stained with 100 µL of Aqua-Glo FITC monoclonal antibody (Waterborne, New Orleans, LA) and incubated in the dark for 30 to 45 min at 37°C. After staining, the suspension was washed with 2 mL of (1x) PST, centrifuged, pipetted down to approximately 100 µL, and the pellet was resuspended. Final volumes of the stained suspension were determined by weight. A 10-µL aliquot of the suspension was then placed in a microscope well, air-dried using a hot air gun, and fixed to the slide well using 10 µL of DAPCO/glycerol mounting medium. A cover slip was placed on the slide and Giardia counts were made at 150x magnification using an epifluorescent microscope. The concentration was determined from the count, well volume, stained suspension volume, and initial volume of the aqueous sample.
Naturally occurring cysts of Giardia in the manure were used in the experiments in the presence of manure suspension. The concentration of cysts of Giardia in the 4 g L–1 manure suspension was determined to be 2.11 x 106 Nc L–1 (Nc denotes the number of cysts) using the enumeration protocol discussed above. Experiments conducted in the absence of manure suspension employed live Giardia lamblia cysts that were obtained from Waterborne (New Orleans, LA). The influent concentration of cysts of Giardia in these experiments was determined to be 8.23 x 106 Nc L–1.
Porous Media
Ottawa aquifer sand (U.S. Silica, Ottawa, IL) was used in the transport experiments. The Ottawa sands will be designated herein by the median grain size (d50) as follows: 710, 360, 240, and 150 µm. The coefficient of uniformity (Ui = d60/d10; here x% of the mass was finer than dx) of the 710-, 360-, 240-, and 150-µm sands was 1.21, 1.88, 3.06, and 2.25, respectively. Ottawa sands typically consisted of 99.8% SiO2 (quartz) and trace amounts of metal oxides, were spheroidal in shape, and had rough surfaces. The vast majority of the sands possessed a net negative charge at a neutral pH. Pore-size distribution information for these Ottawa sands can be calculated from the capillary pressure–saturation curve presented by Bradford and Abriola (2001).
Herzig et al. (1970) calculated the volume of spherical colloids that could be retained in pores based on geometric considerations. The percentage of the total column volume retained by straining was calculated (assuming a porosity of 0.35, a cyst diameter of 10 µm, a grain diameter equal to d10, and the number of contact points between grains to be 7) to be 0.04% for the 710 µm sands, 0.51% for the 360 µm sands, 3.28% for the 240 µm sands, and 5.76% for the 150 µm sands. Although these straining volumes are quite small, significant numbers of cysts are required to fill these sites (Foppen et al., 2005). For example, 2.0 x 1010 cysts (10 µm) would be required to fully saturate (fill) all the straining sites in uniform 150-µm sand packed in a column that is 10 cm long and has an inside diameter of 5 cm. This corresponds to complete retention of cysts of Giardia in 38 142 pore volumes (PV) of suspension at a concentration of 8.23 x 106 Nc L–1.
Column Experiments
Many of the experimental protocols were described in detail by Bradford et al. (2002), only an abbreviated discussion is given below. Borosilicate glass chromatography columns (15 cm long and 4.8 cm i.d.) equipped with a standard flangeless end fitting at the column bottom and a flow adaptor at the top were used in the transport studies. The columns were wet packed with the various porous media, with the water level kept a few centimeters above the soil surface. Table 1 provides porosity (
) values determined according to the method of Danielson and Sutherland (1986) and column lengths for each experimental soil column. A multi-head drive pump was used to pump the tracer suspension (with and without manure suspension) or eluant (0.001 M NaCl) upward through the vertically oriented columns at a steady-rate. Effluent samples were collected in glass test tubes using an autosampler over the course of each experiment, and concentrations of Giardia and manure suspension were measured using the analytical procedures outlined above. The duration of the tracer suspension pulse and the average aqueous Darcy velocity (q) for the various column experiments is given in Table 1.
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A number balance was conducted at the end of each experiment using the Giardia and/or manure suspension effluent and deposition data. The calculated number in the effluent and sand was normalized by the total amount injected into a column. Table 1 presents the calculated percentage recovery in the effluent (Feff), sand (Fsand), and the total system (Ftotal) for the various experimental systems.
Modeling
The HYDRUS-1D computer code (Simunek et al., 1998) was used to simulate the manure suspension and Giardia transport and deposition in the column experiments. Bradford et al. (2003) modified this code to account for colloid attachment, detachment, straining, and size exclusion. HYDRUS-1D is coupled to a nonlinear least squares optimization routine to facilitate the determination of transport parameters from experimental data (effluent and/or deposition data). Aspects of HYDRUS-1D that are relevant to the manure suspension and/or Giardia transport experiments are briefly discussed below.
In the absence of death and/or inactivation processes, the aqueous phase manure suspension or Giardia mass balance equation is written as:
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w [-] is the volumetric water content, JT [Nc Le–2 T–1] is the total flux (sum of the advective, dispersive, and diffusive fluxes) of manure particles or Giardia, and Esw [Nc Le–3 T–1] is the manure particle or Giardia mass transfer terms between the aqueous and solid phases.
Due to the complex physical and chemical nature of the manure suspension and the large size of cysts of Giardia, a simple and flexible 1-site kinetic model formulation for Esw will be employed. This approach lumps straining and attachment deposition processes together and no attempt will be made to separately quantify these mechanisms. The value of Esw is determined as follows:
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b [M Le–3; M denotes mass] is the soil bulk density, S [Nc M–1] is the solid phase concentration of deposited manure particles or Giardia cysts, k1 [T–1] is the deposition rate coefficient, and 
1 [-] is a dimensionless deposition function. The value of 1 is modeled as a function of distance and S as follows:
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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1 to 7.5 PV), C/Ci increased with increasing sand size for a given PV. For a given sand, values of C/Ci also tended to continue to increase with increasing PV. The slope of the breakthrough curve over the 1 to 6 PV range was 0.027, 0.055, 0.072, and 0.035 for the 710-, 360-, 240-, and 150-µm sands, respectively. Hence, the rate of increasing concentration appeared to be greatest for the intermediate grain size sands (240- and 360-µm sand). This time-dependent breakthrough behavior has frequently been ascribed to blocking of favorable attachment sites (e.g., Camesano et al., 1999), but may also be attributed to filling of straining sites (Bradford et al., 2005).
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Figures 1a and 1b also present simulated transport of the manure suspension in the various sands. Table 2 provides a summary of fitted model parameters (dispersivity, 
H; k1; S*max = Smax/Ni where Ni = Ci x 1 mL; and ß), as well as statistical parameters to characterize the goodness of parameter fits. The coefficient of linear regression (Simunek and Hopmans, 2002) estimates the proportion of the variation to effluent (re2) and spatial distribution (rs2) data that is explained by the model. The mean square error for effluent (MSEe) and spatial distribution (MSEs) data is used to quantify the magnitude of the deviation between observed and predicted quantities. Figures 1a and 1b and the statistical parameters in Table 2 indicate that the model generally provided a reasonable description of both effluent and spatial distribution data. Deviations in experimental data and simulations occurred in part due to the simultaneous fitting of effluent and spatial distribution data (see the effluent data for the 360-µm sand in Fig. 1a), and mass balance errors (see Table 1 and the spatial distribution data for the 710-µm sand in Fig. 1b). Lower values of rs2 and higher values of MSEs in Table 2 were also associated with scatter in the spatial distribution data. An improved description of both effluent and spatial distribution data is possible if ß is fitted (Bradford et al., 2003). A fixed value of ß = 0.432 was chosen in these simulations to minimize the number of fitting parameters.
Inspection of Table 2 reveals trends in the fitted model parameters. The value of k1 increased with decreasing sand size, indicating greater deposition (Fig. 1a and 1b). Values of S*max tended to decrease with increasing sand size. This suggests that deposition sites are filled or blocked (time dependency of the breakthrough curves) more rapidly in the coarser-textured sand. A systematic relationship between H and grain size was not found, possibly due to the confounding influence of sand uniformity/gradation or decreased sensitivity of simulation results to this parameter.
To elucidate the mechanisms controlling manure suspension transport and deposition, the particle-size distribution of the influent manure suspension and column effluents was periodically measured. Figure 2 presents the cumulative size distributions (CSDs) of manure particles in the effluent at 95 min (2.5 PV) after passage through the various sands, as well as the CSD for the influent manure suspension. Manure particles larger than around 12, 5, 0.8, and 0.5 µm were completely removed after passage through the 710-, 360-, 240-, and 150-µm sands, respectively, due to mechanical filtration and/or straining. This corresponds to ratios of manure particle to median grain size of 0.003 to 0.017. These ratios are significantly smaller than the straining criterion of 0.18 proposed by Matthess and Pekdeger (1985), but are more consistent with the 0.005 guideline proposed by Bradford et al. (2003).
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Giardia Transport
Figures 4a and 4b present observed and simulated effluent concentration curves and spatial distributions for Giardia in the 710-, 360-, and 150-µm sands in the absence of manure suspension. In this case, very few Giardia were transported through the sands (the value of C/Ci on the y axis of Fig. 4a only goes from 0 to 0.12). Table 1 provides percentage recovery information for Giardia in the effluent and sand, as well as the total system. No Giardia were recovered in the effluent for the 150-µm sand, and only 1.8 and 0.4% were recovered in the effluent for the coarsest 710- and 360-µm sands, respectively. These low percentage recoveries were consistent with the effluent particle-size distribution information for manure particles that was presented in Fig. 2 and 3. Furthermore, the spatial distribution information for Giardia in Fig. 4b was also similar to that shown for the manure particles (Fig. 1b). All of these observations indicate that the deposition of Giardia was controlled by straining, which occurs primarily in the sand adjacent to the column inlet.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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The observed transport and deposition behavior for manure particles has important implications for manure-borne pathogen transport. For the considered experimental conditions, straining of pathogens was likely to occur for values of dp/d50 > 0.003. Furthermore, straining sites were likely to be filled over time as a result of deposition. This last observation indicates that deposition of larger sized pathogens may decrease with time, thus enhancing their transport potential. To further investigate these findings, transport and deposition experiments for cysts of Giardia in the absence and presence of manure suspensions were conducted. In the absence of manure suspension, Giardia had low transport potential and deposition was controlled by straining. For a given sand, higher effluent concentrations of Giardia occurred in the presence than in the absence of manure suspension due to filling of straining sites by manure particles. Hence, pathogen transport studies conducted in the absence of manure suspension may underestimate transport potential in manure-contaminated environments.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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Feff) for Giardia in the presence and absence of the manure suspension is also provided.
