Modeling Transport of Microbes in Ten
Undisturbed Soils under Effluent Irrigation

ORIGINAL RESEARCH

Liping Pang,* Malcolm McLeod, Jacqueline Aislabie, Jirka Šimůnek,Murray Close, and Ross Hector

The HYDRUS-1D mobile–immobile water model (MIM) was used to evaluate the transport of fecal coliforms, Salmonellabacteriophage, and Br in 10 soils. At a flux of 5 mm h−1, a pulse of dairy shed effluent was applied to 30 large undisturbed
lysimeters, followed by water irrigation. Soil types included clayey gley soil, clay loam, silt loam, silt loam over gravels, finesandy loam, dune sand soil, pumice soil, and allophanic soil. Except for dune sand, modeling results showed lower mobile watercontents and dispersivities for microbes than for Br, indicating the exclusion of microbes from smaller pores. The MIM-derived
removal rates were in the order: volcanic soils > greywacke-derived silt loams > granular young sandy soils, and were the mostvariable in clayey gley loam and silt loam over gravels. Microbial reduction was 100% in allophanic soil, 16 to 18 log m−1 inpumice soil (where the unit log is the log10 reduction in maximum concentration compared with the original concentration),
and was lowest in clayey gley soil (0.1–2 log m−1). For most of the other soils, the reduction was 2 to 3 log m−1, except for 9
to 10 log m−1 for fecal coliforms in a fine sandy loam. The detachment rate was only 1% of the attachment rate, indicating
irreversible attachment of microbes. Soil structure (macroporosity) appeared to play the most important role in the transportof microbes and Br, while soil lithology had the greatest influence on attenuation and mass exchange. The general pattern ofpredicted mobile water content agrees with the measured macroporosity, which is positively related to leaching vulnerability but
negatively related to dispersivity.

ABBREVIATIONS: BTC, breakthrough curve; cfu, colony-forming unit, a unit indicating the number of bacteria present in a water sample; DSE,
dairy-shed effluent; PV, pore volume.

I

contamination of waterways by fecal microorganisms may also
adversely affect shellfish harvesting and can pose a health risk torecreational water users. In addition, the health and productivity of livestock may be compromised when they consume watercontaminated with fecal material (Pell, 1997).
Soils act as natural filters that can attenuate microbial contaminants, but they vary widely in their ability to remove them.
The ability of New Zealand soils to remove microorganisms has
been evaluated previously in a few studies. Wells (1973) rated theproperties of New Zealand soils in relation to effluent disposal
and concluded that young (2000–7000 yr of age), fine-grained
tephric soils had the best characteristics for effluent disposal,
while the gleyed soils were unsuitable because of their anaerobic conditions. There were no experimental data to support thisconclusion, however. Childs et al. (1977) performed some lysimeter leaching experiments examining the ability of some New
Zealand soils (peat, clay, silt loam, sandy loam, sand, and stonysoil) to remove chemicals and fecal coliforms from sewage effluent. They found that concentrations of fecal coliforms derived
from effluent were >100 colony-forming units (cfu) L−1 inleachate collected at 50-cm depth for all soils under both sprayand flood irrigation, except for dune sand and a silt loam derived
from volcanic ash under spray irrigation. In a field study of aborder strip (flood) effluent irrigation scheme in Canterbury,
New Zealand, Sinton et al. (2005) observed rapid leaching of
fecal coliforms and F-RNA phages through alluvial gravel soils(15.7–39.2 m h−1), and the estimated reduction in the bacteria
and phages was only log10(cmax/co) = 1.42 and 2.63, respectively(the log10 reduction in maximum concentration compared withrrigation of dairy-shed effluent (DSE) onto land to fertilize pasture and safely dispose of effluent is an integral partof New Zealand’s farming practice; however, the use of inappropriate soils and practices could result in an increased risk ofcontaminating waterways and groundwater with DSE. Animal
wastes contain many pathogenic microorganisms such as
Cryptosporidium, Giardia, Campylobacter, toxigenic Escherichia
coli, Salmonella, and some viruses (e.g., rotavirus) (Pell, 1997),
and some of these are zoonotic (i.e., can cause human diseases).
New Zealand has the highest reported incidence of campylobacteriosis of any developed country (Baker et al., 2006; Gilpin etal., 2006), and there is concern about the possible link between
these outbreaks and contamination of drinking water sources
due to pathogen migration through soil leaching and overland
flow. Apart from harmfully affecting domestic water supplies,
L. Pang, M. Close, and R. Hector, Institute of Environmental Science& Research Ltd, P.O. Box 29181, Christchurch, New Zealand; M.
McLeod and J. Aislabie, Landcare Research, Private Bag 3127, Hamilton, New Zealand; and J. Šimůnek, Dep. of Environmental Sciences,
Univ. of California, Riverside, CA 92507. Received 8 June 2007.
*Corresponding author (Liping.pang@esr.cri.nz).
Vadose Zone J. 7:97–111
doi:10.2136/vzj2007.0108© Soil Science Society of America
677 S. Segoe Rd. Madison, WI 53711 USA.
All rights reserved. No part of this periodical may be reproduced ortransmitted in any form or by any means, electronic or mechanical,
including photocopying, recording, or any information storage andretrieval system, without permission in writing from the publisher.
www.vadosezonejournal.org · Vol. 7, No. 1, February 200897

original concentration), through a 16.8-m vadose zone. In recent
years, lysimeter studies were performed to examine the leaching of fecal coliforms and bacteriophages through a range of key
New Zealand soils commonly used for effluent disposal (Aislabie
et al., 2001; McLeod et al., 2001, 2003, 2004). The results ofthese studies suggest that the vertical movement of bacteria andviruses varies significantly with soil type.
Although experimental data were collected in some of thesestudies, no modeling work was performed. Thus parameters (suchas removal rates) that describe the fate and transport of microbes in
New Zealand soils remains unknown, limiting the applicability ofthe data in the field. Although some overseas studies have derived
parameters of microbial transport in undisturbed soils (Shelton
et al., 2003; Guber et al., 2005; Frazier et al., 2002), the physicochemical properties of some New Zealand soils (e.g., allophanicsoils) are quite unique. In addition, it is difficult to compare theresults from different studies because the removal of microbes insoils changes according to the experimental conditions, especiallythe rate of irrigation (Guber et al., 2005).
Contaminant transport models are useful tools for the quantitative assessment of microbial transport in soils and the elucidationof the importance of factors that control microbial concentrations
in receiving waters. By calibrating transport models with observed
data, we can characterize microbial attenuation and transport ina specific soil system using descriptive parameters (e.g., removal,
attachment, and detachment rates). These calibrated parametervalues together with transport models can then be used by others(e.g., government agencies, regional authorities, researchers, andconsultants) to manage and predict similar systems for various
purposes (e.g., resource management, land-use planning, designof monitoring programs, and risk analysis).
New Zealand has a diverse landscape with a wide range ofcontrasting soil types occurring across short distances (McLeod
et al., 2001). As dairy farming is widespread across the nation,
it is important to evaluate the leaching of microorganisms in the
different soils in New Zealand so that best farming practices canbe implemented. The objectives of this study were (i) to better understand microbial transport in major New Zealand soils
under DSE irrigation, and (ii) to establish values of importantparameters for describing microbial transport and attenuationin these soils by applying an appropriate contaminant transportmodel to the data obtained from lysimeter experiments generated in this and previous studies (Aislabie et al., 2001; McLeod
et al., 2001, 2003, 2004). These results will be of critical importance to regulatory agencies that need scientific information
about microbial removal in different soils to enable them toeffectively manage development and evaluate the risk of groundwater contamination.

mineralogical properties. The major features of the selected soils
are summarized in Table 1, and some physical and chemical
properties are listed in Table 2.
In this study and those by Aislabie et al. (2001) and McLeod
et al. (2001, 2003, 2004), fecal coliforms and a host-specificbacteriophage Salmonella typhimurium 28B (Lilleengen, 1948)
were used as the microbial indicators, and Br was used as a tracer
for water movement. Fecal coliforms are always present in animal and human wastes and are the most widely used bacterialindicator. Fecal coliforms have typical dimensions of 0.3 to 1
μm in diameter and 0.6 to 6 μm in length. The transport offecal coliforms in soils has been reported in many studies (e.g.,
Rahe et al., 1978; McCoy and Hagedorn, 1980; Jamieson et al.,
2002; Unc and Goss, 2003; Shelton et al., 2003). Phage 28B
does not occur in environmental samples or in feces, and it has
been used as a viral tracer to determine the source of fecal contamination (Stenström, 1996). Phage 28B is 60 nm in diameter,
and is persistent at elevated pH values (Carlander and Westrell,1999). Carlander et al. (2000) used Phage 28B to evaluate theimpact of viruses on groundwater quality from wastewater irrigation of a coppice. In their field lysimeter study, rapid transportof Phage 28B was observed in clay soils, with breakthrough at a
depth of 1.2 m after 2 to 24 h, probably due to the presence ofmacropores and bypass flow. They observed that phage transport
through sandy soils varied considerably, with a generally muchslower rate and higher retention compared with the clay soil.
Lysimeters and Leaching Experiments

The methods used for obtaining intact cores of Lismore andTempleton soils and leaching experiments were the same as thoseused for the other soils by Aislabie et al. (2001) and McLeod etal. (2001, 2003, 2004). The description below applies for all 10
soils used for modeling in this study.
Undisturbed soil cores were hand carved in situ from theground surface, and the lysimeter casings were progressively
pressed down over the cores. The lysimeters were made of highdensity polyethylene (HDPE) pipe, with an internal diameter of
46 cm and a length of 47 to 70 cm. A 1-cm internal annulus wasfilled with petroleum jelly to prevent water preferentially flowing at the soil-casing interface. The bottom of the lysimeter was
welded to a 1-cm-thick HDPE base plate, with a sampling port
installed in the center to allow the collection of leachate. The
pore volume (PV) for each set of lysimeter cores was estimatedfrom previous analyses of the total porosity of these soils at thesame site. One PV is the amount of space in the soil core occupied by soil pores or cracks. This ranged from 45 to 67% of thetotal soil volume (Table 2).
In the laboratory, the lysimeters were initially irrigated for 5
d with tap water to field saturation with leachate emanating fromthe sampling port, then were allowed to drain for 7 d. Sevendays is similar to the return period commonly used at effluent
irrigation sites. Following this, each lysimeter was irrigated, at aconstant rate of 5 mm h−1, with a 25-mm depth of DSE, containing native fecal coliforms (typically 105–109 cfu mL−1) andspiked with a tracer solution containing Salmonella bacteriophage (109 plaque-forming units [pfu] mL−1) and Br (2 g L−1).
The lysimeters were then irrigated continuously with tap waterat a rate of 5 mm h−1 using a drip-type rainfall simulator withdrippers spaced on a 20-mm triangular grid, approximately 170

Materials and Methods
Selected Soils and Microbial Tracers

Ten major New Zealand soils were evaluated in thisstudy, including two soils (Lismore silt loam over gravels andTempleton deep silt loam) investigated in this study and eight
other soils presented in Aislabie et al. (2001) and McLeod et al.
(2001, 2003, 2004). These soils are widely distributed in areasof intense dairy farming and are commonly irrigated with DSE.
The selected soils cover a wide range of physical, chemical, andwww.vadosezonejournal.org · Vol. 7, No. 1, February 200898

TABLE 1. Major features of the selected soils.
Soil classification
Soil

Structure

Parent material
New Zealand†

Clay mineralogy

U.S.

Netherton clayey Topsoil: medium or coarse polyhedral structure. Subsoil:
Typic Orthic Gley Typic Endoaquept estuarine
mixed
gley loamcoarse prismatic structure with low porosity within the
alluviumprisms. Large cracks lined with organic matter and clay
cutans, large worm holes and root channels.
Hamilton clay
Topsoil: strongly pedal with fine and medium polyhedral peds. Mottled Orthic
Typic Haplohumult strongly
halloysitic
loam
Subsoil: strongly pedal and clayey. Medium and coarse
Granular
weatheredpolyhedral peds; abundant continuous clay coatings on
rhyolitic andped faces; large nearly vertical earthworm channels
andesitethroughout, up to 5-mm diameter
tephra
Waikiwi silt loam Topsoil: well structured with fine polyhedral peds. Upper
Typic Firm Brown Typic Dystrudept tuffaceous
mixed
subsoil: moderately well developed fine and medium
greywacke
blocky peds. Below 50 cm: firm apedal horizon.
loess
Waikoikoi silt
Topsoil: fine polyhedral structure over a worm-mixed
Fragic Perch-gley Aeric Fragiaquept loess derived
mixed
loam
transitional horizon. Upper subsoil: strongly mottled andPallicfrom schist
well structured with medium blocky peds. About 50 cm:
and greywacke
dense, compact fragipan with very low permeability.
rocks
Lismore shallow Top 36 cm: silt loam, strongly to weakly developed fine to
Typic Orthic
Typic Dystrustept greywacke loess mixed
silt loam overcoarse subangular blocky structure with few indistinct
Brown
on greywacke
gravels
clay coats. 36–70 cm: gravelly silt loam and loamy sand,gravels>50% stones with silt coating. Many fine roots
throughout, very weak soil strength.
Templeton deep Topsoil: very firm with a weakly developed blocky structure
Typic Immature Typic Dystrustept greywacke
mixed
silt loam
over a moderately firm transitional horizon with a weakly
Pallicalluviumdeveloped subangular blocky structure. Upper subsoil:moderately firm with weakly developed coarse blocky
structure. Below about 50 cm: massive soil structure.
Manawatu fineTopsoil: moderately pedal with extremely fine and fine
Weathered
Fluventic
recent soil,
mixed
sandy loam
polyhedral peds. Subsoil: weakly or moderately pedal
Fluvial Recent
Eutrudeptquartzosilt loam and fine sandy loam. Medium polyhedral
feldspathic
peds tending to massive at depth.
alluvium
Typic Sandy
Typic
dune sandmixed
Waitarere recent Minor pedological development with a single-grain structure
sandy soil
throughout, except for some weak aggregation
RecentUdipsammentin the topsoil.
Atiamuri pumice Massive but porous, welded pumice flow tephra at about
Typic Orthic
Typic Udivitrand
sandy rhyolitic
rhyolitic and withsoil
40-cm depth, which prohibits deep rooting by plants.
Pumicetephrasmall fraction
Coarse sand with some gravels, fine to single-grain soilof allophane
structure.
WaihouWeakly developed, porous, subangular blocky and crumb
Typic Orthic
Typic Hapludand rhyolitic tephra
allophanic
allophanic soil
structure. Very fine structure, single grain. Below 40 cm:
Allophanic
welded pumice.

Drainagecapacitypoor

imperfect

good

poor

good

imperfect

good

good

good

good

† New Zealand soil classification (Hewitt, 1998).

TABLE 2. Major chemical and physical properties of the selected soils.
Soil

Layers in
Depth†HYDRUSCpH

TopsoilClay
Subsoil

CEC‡—— % ——

cmolc kg−1

5.4
3.0
4.1
3.2
2.2

0.8
0.8–1.1
1.6–2.7
1.2–1.7

27–32
9.9–17.2
9.1–15.4
9.0–14.2
11.7

0.8

8.3

3.1
2.0

0.3
0.5–0.7

15.2–6.7
8.7–11.3

5.0–5.7

6.0

0.6

5.7–6.2
5.1–6.5

8.1
6.8

0.4
1.7

no.

cm

Netherton clayey soil
Hamilton clay loam
Waikiwi silt loam
Waikoikoi silt loam
Lismore shallow silt
loam over gravels

5
5
4
3
5

70
70
47
50
36

5.1–6.1
4.9–5.3
5.7–6.1
5.9–6.0
5.6

70

5.9

Templeton silt loam
Manawatu fine sandyloam
Waitarere sandy
recent soil
Atiamuri pumice soil
Waihou silty
allophane soil

4
5

40
70

5.6–5.9
5.5–6.4

4

70

4
4

70
70

Subsoil—— % ——

Total θ¶Macropore
θ#

d††
μm

Dp/d‡‡
Fecal
Phagescoliforms—— % ——

0.03
0.05
0.07
0.09
0.21

<2
9
15
14
19§§

73.00
16.11
9.48
10.40
7.68§§

3.00
0.66
0.39
0.43
0.32§§

g cm−3
0.98
1.16
1.22
1.42
1.73

0.61
0.51
0.53
0.45
0.47

12–24

2.20

0.56

24
10

15–23
20

1.37
1.31

0.47
0.49

0.12
0.12

23
75

6.35
1.95

0.26
0.08

3–19

6

2

1.18

0.56

0.19

212

0.69

0.03

5.5–6.2
12–28

5
26

5
34

0.76
0.75

0.50
0.67

0.23
0.16

122
22

1.19
6.67

0.05
0.27

99

52–55
29–30
24
23
21–22

ρ b§

60–69
35–79
12–18
16

† Depth of soil lysimeter taken from ground surface.
‡ Cation exchange capacity.
§ Length-averaged dry bulk density.
¶ Length-averaged porosity.
# Pores ≥59 μm in diameter determined at 5-kPa water potential.
†† Length-averaged mean particle size.
‡‡ Dp = 60 nm for phage and 1.46 μm for fecal coliforms.
§§ 36-cm soil depth only; below 36 cm, gravel size >2 mm.

www.vadosezonejournal.org · Vol. 7, No. 1, February 2008

Topsoil⎛ ∂h⎞⎤∂θ( h )∂ ⎡⎢ K ( h )⎜⎜ + 1⎟⎟⎥
=
⎜
⎝ ∂x
⎠⎟⎥⎦
∂t
∂x ⎢⎣

mm above the soil surface. Typically the chemical properties of
the tap water were as follows: pH = 7.7, electrical conductivity =21.2 mS m−1, and ionic strength = 0.003 mol L−1. Experiments
were performed on triplicate intact cores for each soil type.
To obtain the background levels of Br and microbial tracers in the leachate, samples were first taken at the end of thewetting period. During the leaching experiments, soil leachate
was collected into sterile bottles and subsampled. Subsamples
for microbial assays were stored at 4°C and analyzed within 2 hof collection. Bromide tracer samples were analyzed within 1 wk
of collection.
Batch tests were also performed in the current study todetermine the inactivation rates of the microbial indicators in
DSE under similar experimental conditions to those used in thelysimeter studies (background solution, pH, concentrations of
microbial indicators, and Br). The reactors were incubated at
15°C in the dark for 14 to 17 d. Phages were sampled daily for
14 d, while fecal coliforms were sampled twice a day for the first
5 d and then once a day between Days 5 and 17.

[1]

where h is the water pressure head [L], θ is the volumetric watercontent [L3 L−3], t is time [T], x is the spatial coordinate [L], andK(h) is the unsaturated hydraulic conductivity function [L T−1].
The variable K(h) is described by the van Genuchten–Mualem
hydraulic model (van Genuchten, 1980). The parameters usedin the van Genuchten–Mualem hydraulic model (Table 3) wereobtained by analyzing measured water retention curves (θ vs. h)using the RETC program (van Genuchten et al., 1991) or byusing soil texture data and the Rosetta program (Schaap et al.,2001) if water retention data were absent.
Concentration breakthrough curves (BTCs) for Br are generally asymmetrical with significant tailing. This indicates thepresence of physical nonequilibrium processes in the experimental systems as a result of media heterogeneity. Thus a two-region
mobile–immobile model (van Genuchten and Wagenet, 1989;
Toride et al., 1995) was used to simulate transport of Br:

Sample Analysis

The bacteriophage propagation and assay method
used was detailed in McLeod et al. (2001). Essentially,
Phage 28B was grown overnight on its host strain S.
typhimurium Type 5 in tryptic soy broth at 37°C. The
phages were isolated by chloroform lysis of the bacterial
host, then passed through a 0.45-µm mixed cellulose
ester-based membrane filter to remove cell debris. To
obtain a clean virus preparation free of organic material, the filtrate was centrifuged at 25,000 × g (Sorval
T21, Thermo Fischer Scientific, Waltham, MA) for
2 h at 4°C, the supernatant was poured off, and thephages were resuspended in 1 to 2 mL of phage storage buffer (Sambrook et al., 1989) and stored at 4°C
until required. Phage stocks were enumerated using asoft agar overlay method. Leachate samples were mixed
with the host-strain culture and poured onto nutrient
agar plates. After incubation for 18 to 24 h at 37°C,
well-formed, clear plaques were counted and reported
as plaque-forming units per milliliter. Each reported
phage concentration is the average of three replicates.
Fecal coliforms were determined in soil leachates
using a membrane filtration technique (American
Public Health Association, 1998). Samples werediluted in phosphate-buffered water (pH 7.0), thenfiltered according to standard procedures. The filters
were placed on mFC agar (Difco, BD Diagnostics,
Auckland, NZ) and blue colonies were counted after
incubation for 24 h at 44.5°C. Bromide concentrations in the leachate samples were measured using
an ion-selective electrode (Metrohm 6.0502.100,
Herisau, Switzerland).

TABLE 3. Parameters† used in the van Genuchten–Mualem hydraulic model.
Soil
Netherton clayey gley
loam

Hamilton clay loam

Waikiwi silt loam

Waikoikoi silt loam

Lismore shallow silt
loam over gravels

Templeton deep silt
loam

Manawatu fine sandyloam

Waitarere recent
sandy soil

Atiamuri pumice soil

Modeling and Data Analysis

The Richards equation (Richards, 1931) wasused to describe variably saturated one-dimensionalvertical water flow in the soil lysimeters:www.vadosezonejournal.org · Vol. 7, No. 1, February 2008

Waihou allophanic

Depth
cm
0–10
10–20
20–38
38–49
49–70
0–9
9–19
19–29
29–46
46–70
0–20
20–26
26–39
39–47
0–20
20–41
41–50
0–17
17–28
28–36
36–47
47–70
0–22
22–29
29–34
34–40
0–10
10–23
23–33
33–60
60–70
0–10
10–12
12–30
30–70
0–10
10–23
23–40
40–70
0–15
15–31
31–64
64–70

θr
0.114
0.112
0.116
0.118
0.115
0.090
0.085
0.090
0.099
0.120
0.000
0.000
0.000
0.000
0.000
0.067
0.000
0.078
0.000
0.071
0.041
0.046
0.000
0.076
0.000
0.061
0.000
0.067
0.000
0.073
0.031
0.049
0.050
0.052
0.051
0.235
0.155
0.101
0.149
0.096
0.100
0.109
0.076

θs

α

0.650
0.612
0.616
0.624
0.628
0.532
0.481
0.471
0.500
0.611
0.513
0.462
0.461
0.413
0.430
0.418
0.364
0.476
0.366
0.415
0.243
0.233
0.371
0.445
0.332
0.406
0.457
0.453
0.410
0.451
0.404
0.596
0.451
0.468
0.502
0.547
0.511
0.533
0.568
0.614
0.642
0.670
0.512

cm−1
0.026
0.023
0.027
0.028
0.026
0.008
0.008
0.010
0.014
0.029
0.002
0.001
0.005
0.002
0.003
0.006
0.003
0.005
0.009
0.006
0.045
0.036
0.004
0.006
0.008
0.005
0.004
0.005
0.010
0.005
0.019
0.055
0.041
0.040
0.046
1.338
2.297
1.865
1.756
0.008
0.010
0.015
0.008

n

ρb

1.287
1.287
1.247
1.241
1.263
1.528
1.551
1.479
1.371
1.220
1.267
1.244
1.109
1.112
1.256
1.627
1.148
1.664
1.190
1.628
1.133
1.624
1.204
1.636
1.150
1.688
1.252
1.713
1.191
1.656
1.199
1.499
2.556
2.618
2.492
2.417
2.138
1.827
1.946
1.523
1.503
1.401
1.563

g cm−3
0.870
0.985
1.020
1.005
0.980
1.110
1.210
1.320
1.330
1.030
1.130
1.210
1.290
1.460
1.270
1.500
1.570
1.200
1.353
1.420
2.200
2.200
1.348
1.330
1.510
1.370
1.170
1.245
1.305
1.345
1.420
0.825
0.825
1.290
1.240
0.555
0.745
0.835
0.800
0.775
0.710
0.710
0.995

† θr and θs, residual and saturated water contents; α and n, air-entry parameters in van Genuchten model; ρb, dry bulk density.

100∂θ m c m
∂ ⎛⎜∂c m ⎞⎟ ∂qc m=−α (c m − c im )⎟−⎜⎝θ m Dm⎜∂t∂x∂x ⎠⎟ ∂m
θ im

∂c im
= α (c m − c im )∂t

The inactivation rate for the microbial indicators in the liquid phase (μ) was determined by fitting the experimental data of
the inactivation batch tests with an exponential function, c = coexp(−μt), where co is the influent concentration, using the Solver
function of the Microsoft Excel spreadsheet.
Since an equal flux is applicable for both Br and microbial
tracers, q = (θmvm)microbe = (θmvm)Br, where v is the pore-watervelocity, velocity enhancement of a microbial tracer can be measured from the ratio

[2]
[3]

where the subscripts m and im refer to the mobile and immobile
water regions, respectively; c is the concentration in the liquid
phase [M L−3]; θ = θm + θim is the volumetric moisture content[L3 L−3]; D is the dispersion coefficient [L2 T−1], which is the
product of dispersivity ξ [L] and the spatial coordinate x (i.e., D= ξx); q is the water flux [L T−1]; and α is the first-order massexchange coefficient [T−1] governing the rate of solute exchange
between the mobile and immobile water regions.
The two-region mobile–immobile model (MIM) assumes
that water flow and contaminant transport is limited to themobile water region and that water in the immobile water regionis stagnant, with a first-order diffusive exchange process between
the two regions.
In our recent unpublished batch study, Br was adsorbed insoils that contain volcanic materials (Waihou allophanic soil,
Atiamuri pumice soil, and Hamilton clay loam). Therefore, thedistribution coefficient for linear adsorption, Kd [L3 L−1], wasalso considered for these soils. Assuming all adsorption sites
equilibrate with the mobile water phase, Eq. [2] becomes∂ (θ m + ρ b K d )c m
=
∂t
∂ ⎛⎜
∂c m ⎞⎟ ∂qc m−α (c m − c im )⎟−⎜⎝θ m Dm⎜∂x∂x ⎠⎟ ∂xv m-microbeθ m-Br=v m-Brθ m-microbe

Equations [1–6] were solved numerically using HYDRUS-1D(Šimůnek et al., 2005). The HYDRUS model consisted of four
to five layers for a lysimeter, each with variable inputs of soil
hydraulic properties (using the van Genuchten–Mualem model)
and bulk density. Values of ξ, θm (via θim), and α were optimized for the Br data, while ξ, θm (again via θim), katt, and kdet
were optimized for the microbial data. The measured inactivation rates in the liquid phase for the bacteria and phages, μ, were
fixed in the model. Single values of ξ, θm, α, katt, and kdet wereassigned for all layers. The distinctive transport patterns of Br
and the microbial tracers (Fig. 1), as a result of size exclusion in
microbial transport, meant that ξ and θm for the microbes had
to be independently estimated from those for Br. HYDRUS-1D
was modified for this study to simultaneously assign the samevalues of optimized parameters to all layers and to keep themobile water content the same in all layers. The reason for usingof the same parameter values for multiple layers was to reduce
the number of parameters to be optimized. This treatment isreasonable, as all BTC data were obtained from one sampling
point at the end of the lysimeters.
The available data included 29 Br BTCs, 30 phage BTCs,
and 18 bacteria BTCs (Fig. 1, Table 4). Some BTCs were incomplete, however, and some BTCs had largely zero values. The
quality of the BTCs determined by their completeness is given
in Table 4. Therefore, the number of BTCs suitable for modelingwas 29 for Br, 27 for the phages, and 17 for the bacteria.

[4]in which ρb is the bulk density of the soil material [M L−3]. The
Kd values determined from the unpublished batch study wereused in the model.
We assumed that microbes were excluded from the immobile water region (thus no mass exchange between two regions, α= 0), and thus their attachment and inactivation occurred only inthe mobile water region. Under this assumption, the two-region
MIM for describing transport of microbes at a constant flow isexpressed as∂θ m c m
∂S
+ ρb
=
∂t
∂t
∂ ⎛⎜
∂c m ⎞⎟ ∂qc m− θ m μc m⎟−⎜⎝θ m Dm⎜∂x∂x ⎠⎟ ∂x

Results and Discussion
Transport of Bromide Solute Tracer

Figure 1 shows that the peak concentrations of all of the Br
BTCs arrived earlier than 1 PV except for Waihou allophanicsoil. These earlier Br breakthroughs, together with significant
tailings in the Br BTCs, suggest the presence of preferential flow
paths or dual flow regions due to zones of contrasting permeabilities within the undisturbed cores. When Br passes through thesoil medium, a portion of the solute preferentially goes throughhigh-permeability zones (or the macropore network), providingthat soil moisture is sufficiently high to fill these pores, and theother portion of the solute diffuses into the low-permeability
zones (or matrix). After the solute has moved through the highpermeability zones, the solute in the low-permeability zones
slowly diffuses back to the high-permeability zones, driven by
the concentration gradient. This water exchange between zones
of contrasting permeability causes the observed “tailing” in Br
BTCs. Therefore, the front of a BTC reflects solute transport

[5]

∂S
[6]
= θ m katt c m −ρ b kdet S∂twhere S is the concentration attached to the soil media [cfu or
pfu M−1]; cm is the concentration in the mobile phase [cfu L−3
for bacteria and pfu L−3 for phages]; katt and kdet are the firstorder rate coefficients for attachment and detachment [T−1],
respectively; and μ is the measured first-order inactivation rate
coefficient in the liquid phase [T−1]. We have assumed that theattachment rate, katt, also includes the effects of the air–waterinterface and straining. The total removal rate, ktot [T−1], is thenktot = katt + μ.
ρb

www.vadosezonejournal.org · Vol. 7, No. 1, February 2008

[7]

101

FIG. 1. Concentrations of fecal coliforms, Salmonella bacteriophages, and bromide in the leachate of soil lysimeters (FC = fecal coliforms Pg =bacteriophages). Soils are Manawatu fine sandy loam (MW), Lismore shallow silt loam (LM), Templeton silt loam (TT), Aliamuri pumice soil (AM),
Waitarere sandy recent soil (WT), Hamilton clay loam (HT), Netherton clayey soil (NT), Waihou silty allophane soil (WH), Waikiwi silt loam (WK),and Waikoikoi silt loam (WO); 1, 2, and 3 refer to lysimeter numbers. The pore volumes were calculated based on the total porosity of the soils.
www.vadosezonejournal.org · Vol. 7, No. 1, February 2008

102

FIG. 1. Continued.

through high-permeability zones, while the long tail reflects
solute exchange with low-permeability zones. The presence of
aggregates, earthworm and root channels, and finger flow due
to water repellency is believed to be responsible for the observed
preferential flow in these soils.
In contrast, the peak concentrations of Br BTCs arrived later
than 1 PV in Waihou allophanic soil. This later breakthrough of Br
indicates that Br is not conservative in allophanic soil. Results of abatch test (our recent unpublished data) showed that Br is adsorbed
www.vadosezonejournal.org · Vol. 7, No. 1, February 2008

on Waihou allophanic soil, with a distribution coefficient (Kd) of
0.06 L kg−1 in the top 15 cm of soil and 0.33 L kg−1 in the subsoil(these values were used in the modeling). Sorption of Br in an allophanic soil could be explained by its soil surface charge. Amorphous
allophanic clays have a high isoelectric point of pH 6.0 (Cooper andMorgan, 1979), and Waihou soils have a topsoil field pH that is
typically less than that (Table 2), so the allophane has a net positive
surface charge (McLeod et al., 2001) and thus has an affinity foranions. Sorption of Br in allophanic soils has already been reported
103

TABLE 4. Observed relative transport and concentration reduction of microbes. There wascomplete removal in the Waihou silty allophanic soil with very fine structure.
Exp.†

Microbepore vol.
at cmax‡

Pg1
Pg2
Pg3

0.01
0.01
0.01

Pg1
Pg2
Pg3
FC1
FC2
FC3

0.01
0.01
0.01
0.01
0.01
0.01

Pg1
Pg2
Pg3
FC1
FC2
FC3

0.03
0.06
0.06
0.06
0.06
0.06

Pg1
Pg2
Pg3

0.12
0.12
0.09

Pg1
Pg2
Pg3
FC1
FC2
FC3

0.03
0.03
0.07
0.03
0.03
0.03

Pg1
Pg2
Pg3
FC1
FC3

0.11
0.11
0.08
0.11
0.08

Pg1
Pg2
Pg3
FC1
FC2
FC3

0.24
0.39
0.32
0.67
0.28
0.15

Max. Br pore vol./max. microbepore vol.

cmax/coSpatialRemoval Quality oflog(cmax/co)coordinate
rate
BTC§

m
Netherton clayey soil (no bacteria data available)
2.30
8.25 × 10−1
0.70
0.08
9.40
3.25 × 10−1
0.70
0.49
7.30
3.50 × 10−2
0.70
1.46
Hamilton clay loam
86.54
3.13 × 10−2
0.70
1.50
20.90
7.70 × 10−2
0.70
1.11
50.77
6.94 × 10−2
0.70
1.16
86.54
6.07 × 10−3
0.70
2.22
0.70
1.87
20.90
1.36 × 10−2
50.77
3.51 × 10−2
0.70
1.45
Waikiwi silt loam (no Br data available for Lysimeter 3)
10.32
7.59 × 10−2
0.47
1.12
7.81
7.80 × 10−2
0.47
1.11
0.47
0.97
7.81
1.07 × 10−1
6.19
7.87 × 10−2
0.47
1.10
7.81
8.54 × 10−2
0.47
1.07
7.81
4.88 × 10−2
0.47
1.31
Waikoikoi silt loam (no bacteria data available)
6.47
7.68 × 10−2
0.50
1.11
6.91
4.51 × 10−2
0.50
1.35
7.12
9.02 × 10−2
0.50
1.04
Lismore shallow silt loam over gravels
6.37
2.02 × 10−1
0.70
0.69
8.11
2.00 × 10−2
0.70
1.70
0.70
1.77
5.60
1.69 × 10−2
6.37
2.02 × 10−2
0.70
1.69
8.11
5.75 × 10−3
0.70
2.24
13.52
2.86 × 10−5
0.70
4.54
Templeton silt loam
4.72
9.50 × 10−2
0.40
1.02
3.86
1.81 × 10−1
0.40
0.74
3.80
2.39 × 10−1
0.40
0.62
4.72
1.90 × 10−1
0.40
0.72
3.80
3.07 × 10−1
0.40
0.51
Manawatu fine sandy loam
2.18
5.19 × 10−3
0.70
2.28
1.47
2.08 × 10−2
0.70
1.68
1.91
5.10 × 10−3
0.70
2.29
0.80
6.07 × 10−7
0.70
6.22
0.70
6.69
2.03
2.02 × 10−7
3.94
2.02 × 10−7
0.70
6.69
Waitarere sandy recent soil (dune sand)−2
0.72
2.06 × 10
0.70
1.69
0.61
3.51 × 10−2
0.70
1.45
0.70
2.02
0.86
9.49 × 10−3
0.72
2.50 × 10−2
0.70
1.60
0.61
4.27 × 10−2
0.70
1.37
0.86
1.15 × 10−2
0.70
1.94
Atiamuri pumice soil (no bacteria data available)
1.84
2.33 × 10−12
0.70
11.63
0.70
12.22
1.37
6.00 × 10−130.76
9.44 × 10−12
0.70
11.03

log¶ m−1
0.12
0.70
2.08

poor
poor
poor

2.15
1.59
1.66
3.17
2.67
2.08

poor
poor
poor
poor
poor
poor

2.38
2.36
2.07
2.35
2.27
2.79

good
good
good
good
good
good

2.23
2.69
2.09

good
good
good

0.99
2.43
2.53
2.42
3.20
6.49

poor
poor
good
poor
poor
poor

2.56
1.85
1.56
1.80
1.28

good
good
ok
good
ok

3.26
2.40
3.28
8.88
9.56
9.56

poor
ok
good
poor
poor
poor

soil type. The MIM-derived dispersivity for Br
transport (Table 5) is on average 7% of the lysimeter length (SD = 6%, n = 29). Although there
is a lot of variability in the data, dispersivity ofBr transport appears to be inversely correlatedwith the measured macroporosity (Fig. 3). This is
expected, as with an increase in macropores in thesoils, convection flow would be more dominant
and less dispersion would occur.
The fraction of mobile water, θm/θ, (Table 5)accessible for Br transport is on average 0.45 (SD= 0.23, n = 29). The θm/θ values are lowest for
Netherton clayey soil and Hamilton clay loam,
implying that, in highly heterogeneous soils, onlya small fraction of water is needed to leach solutecontaminants. This suggests that the fraction ofmobile water reflects the degree of soil heterogeneity. The fact that the pattern of model-predictedmobile water content agrees with measured macroporosity (Fig. 3) also supports this comment.
The mass exchange rate, α, (Table 5) ismuch higher for allophanic and pumice soils
than for other soils, indicating that Br transport
is not at equilibrium in volcanic soils. In contrast,
the α value is close to zero for dune sand, suggesting that Br transport in uniform dune sandwas under equilibrium conditions. The relatively
symmetric shape of Br BTCs with little tailingfor this soil also supports this conclusion. The
relationship between α and macroporosity is notclear in this study (Fig. 3).
Transport of Fecal Coliforms andBacteriophages
Breakthrough Curves

The BTCs of microbial tracers show a very
different pattern from those of Br (Fig. 1). In comPg1
0.26
2.41
good
parison with Br, the BTCs of microbial tracers comPg2
0.37
2.08
good
monly peak much earlier and are much less spread
2.89
good
Pg3
0.26
FC1
0.26
2.29
good
out. Many others (e.g., Shelton et al., 2003; Guber
FC2
0.37
1.96
good
et al., 2005; Levy et al., 2007) have also observed an
FC3
0.26
2.77
good
earlier breakthrough (or velocity enhancement) of
Pg1
0.37
16.62
poor
microbes than conservative solutes in undisturbed
17.46
poor
Pg2
0.42
soils. Except for Waitarere dune sand and phages in
Pg3
0.89
15.75
ok
one lysimeter in Atiamuri pumice soil, all microbial† Pg, bacteriophages; FC, fecal coliforms; 1, 2, and 3 refer to lysimeter numbers.
BTCs finished ahead of the front of the Br BTCs.
‡ c = concentration.
§ Determined by the completeness of the breakthrough curve (BTC).
This suggests that microbes are transported through¶ The unit log is log10 reduction in maximum concentration compared with the original concentration,a macropore network and that the soil matrix has
log10(cmax/co).
little impact on their transport. Similarly, others have also commented that microbial transport(Close et al., 2003). Although Br was also adsorbed in Atiamuri
occurs primarily through interconnected large pores (Wollum andpumice soil (Kd = 0.01 L kg−1 for topsoil and 0.03 L kg−1 for subCassel, 1978) and almost follows a piston flow (Germann et al.,soil) and Hamilton clay loam (Kd = 0.00 for topsoil and 0.03 L kg−1
1987). The effect of macropores on colloid transport in intact coresfor subsoil), the degree of adsorption was not high enough to cause
was also suggested in the review of DeNovio et al. (2004).
a shift in the concentration peak.
Figure 4 shows that MIM-simulated BTCs fit well the
Model-simulated Br concentrations are compared withobserved data. As it is superfluous to present all model-simulated
BTCs here, we present only one lysimeter for one soil type inobserved concentrations in Fig. 2, selecting one lysimeter per

www.vadosezonejournal.org · Vol. 7, No. 1, February 2008

104

FIG. 2. Comparison of observed andmobile–immobile model (MIM) simulated
Br concentrations in the leachate of soil
lysimeters. Circles are observed dataand solid lines are model-simulated
data. Soils are Waikiwi silt loam (WK),
Waikoikoi silt loam (WO), Lismore shallow silt loam (LM), Templeton silt loam(TT), Manawatu fine sandy loam (MW),Waihou silty allophane soil (WH), Waitarere sandy recent soil (WT), Aliamuri
pumice soil (AM), and Netherton clayeysoil (NT); 1, 2, and 3 refer to lysimeter
numbers.

Fig. 4, which was typical (representative) of other BTCs.
Double peaks are displayed in
the bacteria BTCs of Hamilton clay
loam and the phage BTCs of Atiamuri
pumice soil, with the first peaks showing velocity enhancement and second
peaks showing later arrival than Br.
The first peaks of the bacteria BTCs
of Hamilton soil are concurrent withthose of phages that do not show any
second peak. As the concentrations of
the bacteria in the second peaks areabout two orders of magnitude lower
than those of the first peaks, they are
not noticeable on the scale shown in
Fig. 1. For the pumice soil, the firstpeak was the major peak in one column and the minor peakin another column. Multiple peaks in a microbial BTC suggest
the presence of multiple flow paths of contrasting permeability
for microbial transport within the heterogeneous medium or
detachment of adsorbed microbes associated with a change inleaching conditions. As leaching conditions were stable, multiple
flow paths are the probable explanation.

TABLE 5. Parameters† derived from Br breakthrough curves using the
HYDRUS mobile–immobile model (MIM).
Soil

Netherton clayey
gley loam
Hamilton clay loam

Waikiwi silt loam‡
Waikoikoi silt loam

Lismore shallow
silt loam overgravels
Templeton deep
silt loam
Manawatu fine
sandy
loam
Waitarere recent
sandy soil
Atiamuri pumicesoil
Waihou allophanic

Lysimeter

1
2
3
1
2
3
1
2
1
2
3
1
2
3
1
2
3
1
2
3
1
2
3
1
2
3
1
2
3

Optimized from MIM
ξ
cm
10.00
4.00
6.50
9.32
4.76
7.62
11.87
9.54
4.16
2.37
7.69
6.01
6.77
4.18
3.00
2.61
4.30
0.40
0.35
0.13
5.07
3.00
5.00
0.43
0.22
0.88
1.00
1.79
0.74

θm

α

Calculated
r2

θm/θ

ξ/L

0.92
0.87
0.83
0.94
0.91
0.39
0.97
0.99
0.99
0.99
1.00
0.97
0.95
0.86
0.93
0.91
0.91
0.97
0.95
0.94
0.98
0.95
0.99
0.97
0.95
0.93
0.98
0.98
0.93

0.11
0.15
0.15
0.15
0.15
0.15
0.84
0.84
0.53
0.32
0.74
0.36
0.38
0.50
0.45
0.49
0.51
0.50
0.51
0.52
0.46
0.46
0.47
0.80
0.84
0.80
0.20
0.20
0.41

0.14
0.06
0.09
0.13
0.07
0.11
0.25
0.20
0.08
0.05
0.15
0.09
0.10
0.06
0.08
0.07
0.06
0.01
0.01
0.00
0.07
0.04
0.07
0.01
0.00
0.01
0.01
0.03
0.01

d−1
0.07
0.10
0.10
0.08
0.08
0.08
0.43
0.43
0.23
0.14
0.32
0.17
0.18
0.24
0.17
0.18
0.19
0.23
0.23
0.24
0.28
0.28
0.28
0.44
0.46
0.44
0.12
0.13
0.25

0.21
0.15
0.43
1.14
0.67
0.93
0.15
1.20
1.23
1.73
1.20
0.08
0.12
0.21
1.85
0.85
0.53
0.27
0.26
0.28
0.00
0.00
0.01
2.36
0.34
3.82
3.76
4.00
3.76

Mobile–Immobile Water, Velocity Enhancement

In comparison with Br, the fraction of mobile water, θm/θ(Table 6), is much smaller for microbial BTCs that exhibit velocity
enhancement (i.e., excluding Waitarere sandy recent and Atiamuri
pumice soil), on average only 0.19 (SD = 0.09, n = 29), in a narrow range of 0.08 to 0.24, except for Manawatu fine sandy loam
(0.40–0.45). This is because microbes can only access a smaller
range of larger pores due to size exclusion, unlike the Br solute,
which can access a wider range of pore sizes. Slower velocity zones
near the solid surfaces, which are accessible to Br and might beconsidered mobile for Br, would become inaccessible to microbes
and would thus be treated as immobile. Water will then travel
faster if going through a smaller porosity. Shelton et al. (2003)
estimated that the porosity available for fecal coliform transport
in undisturbed stony silt loam is 15% of the total water content,
which is similar to our findings. In contrast, θm/θ is much larger
for microbial BTCs that arrived later than Br (Table 6), on average
0.80 (SD = 0.10, n = 7). Like the results from Br, the pattern ofpredicted mobile water content agrees with the measured macroporosity (Fig. 3).

† Data for Waikiwi silt loam Lysimeter 3 were not available.
‡ ξ, dispersivity; θm, mobile water content; L, column length; θ, total porosity; α,mass exchange rate between two regions.

www.vadosezonejournal.org · Vol. 7, No. 1, February 2008105

ing from 90-cm-long undisturbed stony soil
was about seven times greater than the average pore velocity.
The above relative speed, as measured
by the θm-Br/θm-microbe ratio, relates to themean velocity or center of mass. If the relative speed is examined using the ratio of porevolume at peak concentration of Br to thatof a microbial tracer (Table 4), which reflects
macropore velocity (De Jonge et al., 2004),
the relative speed for microbial transport ismuch greater than for Br. It is in the order ofHamilton clay loam (21–87) > Lismore shallow silt loam over gravels, Waikiwi silt loam,
and Waikoikoi silt loam (6–14) > Templeton
silt loam (4–5) > Manawatu fine sandy loam
and Atiamuri pumice soil (1–2) > Waitarere
sandy recent soil (<1). The ratio for heterogeneous Netherton clayey soil varies between
2 and 9.
The θm-Br/θm-microbe ratios for
Waitarere dune sand were <1 (Table 7),
suggesting that the transport velocity of
microbes in Waitarere dune sand was slower
than that of Br. This is probably because thissoil has only minor pedological development, with a single-grain structure throughout. It is therefore more uniform than othersoils, thus matrix flow plays an importantrole in microbial transport in the dune sand.
The θm-Br/θm-microbe ratio was also <1 forone lysimeter of Atiamuri pumice soil, suggesting that transport of phages was slower
than that of Br in one of the pumice soil
lysimeters.
Dispersion

Dispersivity values derived from mostmicrobial BTCs (Table 6) are much smaller
than those from Br BTCs (average ξBr/
ξmicrobe = 4.69, SD = 3.85, n = 35, Table7) as a result of a narrower pore network
involved in microbial transport. The lower dispersion in microbial transport compared with solute transport was also observedin the lysimeter study of Shelton et al. (2003) with an undisturbed silt loam. There are a few exceptions of greater ξ values
for microbes than for Br, but this is believed to be an artifact of
the erratic data for microbial BTCs.
The dispersivity/transport distance ratio for microbe transport was less than that for Br, on average 5% (SD = 6%, n = 36,
Table 6), mostly ranging from 1 to 3%. As for Br, the dispersivity of microbe transport appears to be inversely correlated withmacroporosity (Fig. 3).

FIG. 3. Correlations of macroporosity with transport parameters.

The θm-Br/θm-microbe = vm-microbe/vm-Br ratios derived fromMIM (Table 7) suggest that the transport of the microbes wasalways faster (mostly two to four times) than that of Br, except in
Waitarere dune sand and one lysimeter of Atiamuri pumice soil.
This indicates that velocity enhancement is a common phenomenon in the structured soils investigated here because the microbes
are excluded from smaller pores in the soil medium. The degreeof velocity enhancement, as measured by θm-Br/θm-microbe, is in
the order of: Waikiwi silt loam (4) > Lismore shallow silt loam,
Waikoikoi silt loam, and Templeton silt loam (2–4) > Hamilton
clay loam, Manawatu fine sandy loam, and Netherton clayey soil
(1–2) > Waitarere sandy recent soil (<1). For a particular lysimeter,
there was little difference in speed between bacteria and phages asreflected in their similar θm-Br/θm-microbe ratios (Table 7). Ourfinding on the faster velocity of microbes than Br is similar to theobservation of Shelton et al. (2003), who conducted a lysimeter
study. They found the average velocity of coliform bacteria leach-www.vadosezonejournal.org · Vol. 7, No. 1, February 2008

Leaching Vulnerability of Fecal Coliforms
and Bacteriophages

The PV at maximum concentration (cmax) (Table 4), thenormalized volume of water required for reaching maximum concentration in the leachate, reflects the leaching vulnerability of106

microbes through soils. The leaching vulnerability for microbes
is in the order of: Netherton clayey soil and Hamilton clay loam
(0.01) > Lismore shallow silt loam over gravels (0.03) > Waikiwi
silt loam (0.06) > Templeton silt loam and Waikoikoi silt loam
(0.08–0.12) > Manawatu fine sandy loam, Waitarere dune sand,and Atiamuri pumice soil (0.24–0.89) > Waihou allophanic soil
(not leached). This sequence is consistent with a general trend of
decreasing heterogeneity of soil structure. This suggests that heterogeneous soils, due to the presence of preferential flow paths, aremore vulnerable to microbial leaching through soils. The small PV
values at cmax (Table 4) suggest that, in structured heterogeneous
soils, even a very small amount of water in the unsaturated soils
could lead to a rapid and significant leaching of microbes throughbypass flow. This result suggests that the leaching vulnerability of
microbes into shallow water bodies could be the greatest in clayeysoils, which often crack, followed by silt loam over gravels, silt
loam, sandy loam, dune sand, pumice soil, and allophanic soil.
Figure 3 shows that there is a positive relationship between macroporosity and leaching vulnerability of microbes.
Removal of Fecal Coliforms and Bacteriophages
Reduction in Concentration and Mass

The greatest reduction in phage concentration was observedin Waihou allophanic soil—no phages were detected in theleachate from this soil. As mentioned above, previous studies
have suggested that allophanic clays have a net positive charge inthe topsoil, which prompts bonding of negatively charged phages.
In addition, allophane has a verylarge surface area, 700 to 900 m2
g−1 (Aislabie et al., 2001), further
enhancing the bonding of phages
with the soil medium. The second
greatest reduction in phage concentrations occurred in the Atiamuri
pumice soil [16–18 log m−1, where
the unit log is log10(cmax/co), Table
4]. The presence of allophanic clay,
even though just a small fraction in
the pumice soil (Table 1), is believed
to have played an important role inremoval of phages in Waihou allophanic soil and Atiamuri pumicesoil.
For most other soils, thereduction in fecal coliform andphage concentrations is about 2 to
3 log m−1 (Table 4), except for agreater removal of fecal coliforms
in Manawatu fine sandy loam (9–10 log m−1). The clayey gley soil
had the least reduction in microbial concentration (0.1–2 log m−1).
This finding agrees with the inference of Wells (1973) that tephricsoils have the best characteristics
for effluent disposal, and soils withcracks, such as gley soils, are notsuitable for effluent disposal.
Attachment and Removal Rates

FIG. 4. Comparison of observed and simulated concentrations of fecal coliforms (FC) and Salmonellabacteriophages (pg) in the leachate of soil lysimeters. Empty dots are observed data. The red solid lines
are data fitted with the mobile–immobile model. Soils are Lismore shallow silt loam (LM), Templeton
silt loam (TT), Manawatu fine sandy loam (MW), Waitarere sandy recent soil (WT), Hamilton clay loam(HT), and Netherton clayey soil (NT); 1, 2, and 3 refer to lysimeter numbers.
www.vadosezonejournal.org · Vol. 7, No. 1, February 2008

107

The MIM-derived katt rates(Table 6) are the highest for thesoils of volcanic origin (complete
removal in Waihou allophanic soil,
11–12 d−1 for Atiamuri pumicesoil and Hamilton clay loam). The
high level of attachment associatedwith volcanic soils is attributed
to their large surface areas, which
are variably charged, as discussed
above. Silt loams of greywacke ori-

gin (Templeton silt loam, Waikoikoi silt loam, and Waikiwi silt
air–water interaction effects could not be quantified. The effectsloam) have the second highest katt rates, ranging from 7 to 10of these processes are combined in the total removal rates. We
d−1. In these soils, soil particles are often coated with a thin layer
could only identify the possible presence of these processes.
of Fe and Mn oxides, which promote attachment of microbes.
Straining occurs when the ratio of the colloid to medium
The lowest katt rates are found for the granular young soils (1–3
grain diameter, Dp/d, is >0.5% (Bradford et al., 2004), and will
d−1 for Waitarere dune sand soil, 4–5 d−1 for Manawatu finebe significant when the ratio is >8% (McDowell-Boyer et al.,sandy loam). This is expected because granular soils are generally1986). Using these criteria, straining may be expected in theweaker adsorbents for microbes than clays and minerals (Sobsey
transport of fecal coliforms through all of the lysimeters (Dp/det al., 1980; Moore et al., 1981). In addition, much less coating> 0.69%, Table 2), and could be significant in clayey soil, clay
is present on the grain (largely silica) surfaces of these young
loam, and silt loam (Dp/d ≥ 10%). Based on these criteria, strainsoils. Heterogeneous soils have the most variable katt rates (1–16
ing may have also occurred in the transport of phages in clayey
d−1 for Netherton clayey gley loam, 5–26 d−1 for Lismore shalsoil and clay loam (Dp/d = 0.7–3%). It should be noted that thelow silt loam), probably due to an uneven distribution of readcriteria for straining described above were developed from media
ily available attachment sites. The explanation for their possiblywith uniform grain sizes and that these criteria do not consider
high katt rates is that clays and metal oxides have a strong affinity
the effect of soil aggregates and macropores. Although the grain
for microbes. In Lismore silt loam over gravels, >50% of thediameter may be small in aggregated soils, the effective diamstones (derived from greywacke) show coatings. The relationeter may be a lot larger because the grains are clumped and theship between katt and macroporosity is not clear (Fig. 3). Thesemicrobes are not interacting with single grains. The large interresults suggest that attachment and thus removal of microbes
connected macropores developed in aggregated soils could allow
is predominantly influenced by soil chemistry, particularly thethe rapid transport of microbes with little straining. Therefore,
lithologic origin.
the effect of soil aggregation and macropores on straining is
The above patterns are also applicable for ktot rates deterunknown, especially for clayey soils, which naturally develop
mined from MIM (Table 6). The ktot rates
derived from MIM are the highest in soils of TABLE 6. Transport parameters† derived from bacteriophage (Pg) and fecal coliform (FC)breakthrough curves using the HYDRUS mobile–immobile model (MIM).
volcanic origin (allophanic soil > 0.51 h−1,
Optimized from MIM
Calculated−1
pumice soil 0.51 h , and clay loam containSoil
Microbe Lysimeter
ξ
katt
kdet
r2
θm/θ
ξ/L
ktot
kdet/kattθm−1
ing tephra 0.48–0.52 h ), second in silt
−1
−1
−1
−1
cm
d
d
h
loams of greywacke origin (0.30–0.43 h ),NethertonPg
1
1.63 0.05
1.21 0.19 0.81 0.08 0.02 0.06
0.153
weakest in granular young sandy soils (fineclayey2
10.00 0.05
5.23 0.13 0.87 0.08 0.14 0.23
0.026
−1
gley loam
sandy loam 0.17–0.23 h , dune sand soil
3
5.00 0.08 16.18 0.36 0.37 0.12 0.07 0.68
0.022
0.07–0.15 h−1), and the most variable in het- HamiltonPg1
8.92 0.14 12.21 0.10 0.98 0.24 0.13 0.52
0.008
clay loam
erogeneous soils (clayey gley loam 0.06–0.68
2
10.00 0.10 11.28 0.04 0.99 0.17 0.14 0.48
0.003
315.00 0.10 11.58 0.05 0.99 0.17 0.21 0.49
0.004h−1, silt loam over gravels 0.23–1.09 h−1).
Waikiwi siltPg
1
7.60 0.10
9.02 0.11 0.87 0.19 0.16 0.38
0.012
−1The kdet rate (mean 0.08 d , SD =loam
2
4.16 0.10
8.91 0.04 0.87 0.20 0.09 0.38
0.005
0.07, n = 36, Table 6) is on average only 1%
3
3.28 0.10
8.50 0.03 0.54 0.19 0.07 0.36
0.004
FC
1
5.74 0.10
9.54 0.06 0.77 0.19 0.12 0.41
0.006
of the katt rate (mean 8.28 d−1, SD = 4.95,
2
3.90 0.10
9.85 0.19 0.60 0.19 0.08 0.42
0.019
n = 36). The very low kdet rates suggest that3
4.26 0.10
9.90 0.07 0.74 0.19 0.09 0.43
0.007
detachment of microbes in the structured WaikoikoiPg10.74 0.08
7.91 0.04 0.97 0.19 0.01 0.34
0.005
silt loam
20.44 0.08
9.91 0.02 1.00 0.18 0.01 0.42
0.002
soils investigated here was negligible and that3
1.00 0.08
7.15 0.06 0.94 0.19 0.02 0.31
0.008
microbial attachment could be considered to LismorePg
1
0.88 0.06
5.31 0.02 0.93 0.12 0.01 0.23
0.004
be irreversible. Other researchers have also
shallow2
1.19 0.07 10.11
0.02 0.98 0.15 0.02 0.43
0.002
silt loam
30.44 0.08
8.64 0.03 0.93 0.17 0.01 0.37
0.003
commented that microbial attachment to
over
FC
1
0.42 0.05 13.71 0.06 0.98
0.11
0.01 0.58
0.005
porous media is primarily an irreversible progravels
20.49 0.06 17.12 0.06 0.77 0.12 0.01 0.73
0.004
cess (Yao et al., 1971; Rajagopalan and Tien,
3
0.72 0.08 25.79 0.10 0.69 0.17 0.01 1.09
0.004
TempletonPg
10.45 0.07
7.38 0.07 0.93 0.20 0.01 0.32
0.009
1976; Pieper et al., 1997).
Relative Contribution of Individual Processes

deep silt
loam

2
3
1
3
1
2
3

FC

The inactivation rate derived from thebatch incubation tests conducted at 15°C
(a similar temperature to that used in thelysimeter experiments) was 0.298 d−1 forfecal coliforms and 0.214 d−1 for the phages.
The contribution of inactivation to the total
removal rate was, on average, 3.78% forphages (SD = 3.17%, n = 25) and 5.54% forfecal coliforms (SD = 5.34%, n = 11).
Although the contribution of inactivation to total removal could be examined, theindividual contributions of straining andManawatu
fine
sandy
loam
Waitarere
recentsandy
soil

Atiamuripumice
soil

Pg

Pg

1
2
3
1
2
3
3

FC

Pg

0.56
0.60
0.39
0.30
0.13
0.07

0.06
0.05
0.06
0.05
0.18
0.21

8.15
7.49
8.00
6.84
5.41
3.94

0.06
0.10
0.08
0.09
0.18
0.02

0.92
0.94
0.90
0.93
0.80
0.53

0.15
0.14
0.16
0.12
0.40
0.45

0.01
0.01
0.01
0.01
0.00
0.00

0.35
0.32
0.35
0.30
0.23
0.17

0.008
0.013
0.011
0.013
0.033
0.006

0.00
0.67
2.38
2.20
2.38
2.33
2.04
0.45

0.20
0.42
0.48
0.46
0.45
0.48
0.46
0.55

5.35
2.91
1.58
3.37
2.10
1.36
3.19
11.98

0.00
0.07
0.00
0.03
0.02
0.01
0.04
0.18

0.86
0.88
0.90
0.78
0.95
0.89
0.77
0.49

0.43
0.70
0.81
0.77
0.76
0.81
0.76
1.00

0.00
0.01
0.03
0.03
0.03
0.03
0.03
0.01

0.23
0.13
0.07
0.15
0.10
0.07
0.15
0.51

0.000
0.024
0.003
0.008
0.009
0.006
0.011
0.015

† ξ, dispersivity; θm, mobile water content; θ, total porosity; L, column length; katt, attachment rate; kdet,
detachment rate; ktot, total removal rate.

www.vadosezonejournal.org · Vol. 7, No. 1, February 2008108

cracks within the soil. This could not be assessed in this study as
no attachment profiles were measured during the experiments.
The air–water interface plays an important role in theenhanced removal of microbes under unsaturated conditions compared with saturated conditions (Chu et al., 2003;
Torkzaban et al., 2006). Retention of microbes increases as watercontent decreases (Jin et al., 2000; Han et al., 2006; Torkzaban
et al., 2006). Evaluating the effect of the air–water interaction
is difficult in this study, however, as water contents were notmeasured.

this was in uniform, single-grain dune sand, where the velocity
of microbial tracers was slower than that of Br.
Breakthrough of both microbes and Br occurred at PV <<1, suggesting that rapid and significant leaching of microbial andsolute contaminants could occur through bypass flow in structured soils with a small amount of water. An exception is for the
allophanic soil, in which Br was adsorbed and the concentration
peaked at >1 PV. Leaching vulnerability seems to relate to soil
heterogeneity, being greatest in clayey and clay soils with cracks,
followed by silt loam over gravels, silt loams, sandy soil, dunesand soil, pumice soil, and allophanic soil.
For both Br and the microbes, the general pattern of predicted mobile water content agrees with measured macroporosity, which is positively related to leaching vulnerability but negatively related to dispersivity. This suggests that soil structure plays
the most important role in the transport of microbes and Br.
The relationship between macroporosity and the mass exchange
rate, however, was not clear in this study. The mass exchange
rate between mobile and immobile water regions was greatest in
volcanic soils and lowest in granular, young sandy soils.
Soil lithology has the greatest influence on the attenuationof microbes (attachment, removal, and reduction). The relationship between the attachment rate and macroporosity is notclear. The total removal rates (the sum of attachment rate andinactivation rate) derived from the MIM were highest in soilsof volcanic origin (allophanic soil >0.51 h−1, pumice soil 0.51
h−1, and clay loam containing tephra 0.48–0.52 h−1), second
highest in silt loams of greywacke origin (0.30–0.43 h−1), lowest in granular, young sandy soils (fine sandy loam 0.17–0.23
h−1, dune sand soil 0.07–0.15 h−1), and most variable in heterogeneous soils (clayey gley loam 0.06–0.68 h−1, silt loam overgravels 0.23–1.09 h−1).
The reduction in microbial concentration was the greatest in the allophanic soil (total removal) and second greatest in
the pumice soil (16–18 log m−1). The least reduction in phage
concentrations occurred in clayey gley soil (0.1–2 log m−1). For
most other soils, fecal coliforms and phages had a concentration
reduction of about 2 to 3 log m−1, except that the fine sandy loam
had a greater concentration reduction for fecal coliforms (9–10
log m−1). These removal rates represent a reduction in microbialconcentration on a natural log scale, and it needs to be divided
by a factor of 2.3 to convert them to log10. The detachment
rate of microbes was, on average, only 1% of the attachment
rate, suggesting that detachment of microbes was negligible andattachment of microbes could thus be treated as irreversible.
The results of data analysis and modeling obtained inthis study help our understanding of leaching vulnerability of
microbes and the efficiency of effluent treatment for microbial
removal in different soil media. We believe that this information could be applicable for soils under similar conditions, andthat the results summarized from this study could provide useful
information to regulatory agencies to more effectively manage
land use and development and evaluate the risk of groundwatercontamination.
These results, however, are applicable only for soils above thevadose zone (the zone between the soil root zone and the groundwater table). The ability of the vadose zone to remove microbes
is expected to be much less effective. Thus, the reduction rates
derived from soils cannot be extrapolated to vadose-zone media,

Conclusions
Our modeling results showed generally smaller valuesof mobile water content and dispersivity for microbial tracers
compared with Br. This indicates that the transport of microbes
in highly structured soils is predominantly controlled by macropores because they are excluded from small pores, resulting in the observed earlier breakthrough than Br (i.e., velocity
enhancement). Thus transport of microbes is commonly moreconvective and less dispersive than that of Br. An exception to

TABLE 7. Relative movement of bacteriophages (Pg) and fecal coliforms (FC) related to Br.
Soil

Microbe Lysimeter θm-Br/θm-micro† ξBr/ξmicro†
Earlier arrival than Br

Netherton clayey gley loam

Pg

Hamilton clay loam

Pg

Waikiwi silt loam

PgFC

Waikoikoi silt loam

Pg

Lismore shallow silt loam
over gravels

Pg

FC

Templeton deep silt loam

Pg

FC
Manawatu fine sandy loamPg

Waitarere recent sandy soil

Pg

1
2
3
1
2
3
1
2
3
1
2
3
1
2
3
1
2
3
1
2
3
1
2
3
1
3
1
2
3

1.44
2.00
1.25
1.04
2.34
2.11
4.33
4.19
4.31
4.33
4.31
4.31
2.81
1.83
3.87
3.01
2.53
2.87
3.42
3.16
2.96
2.32
3.20
3.65
2.79
4.09
1.24
1.13
1.20

6.14
0.40
1.30
1.05
0.48
0.51
1.56
2.29
2.91
2.07
2.45
2.24
5.60
5.40
7.69
6.82
5.67
9.49
14.22
13.74
5.82
6.59
4.65
7.16
7.71
14.18
3.10
4.81
–

Later arrival than Br

FC

Atiamuri pumice soil

Pg

1
2
3
1
2
3
3

0.66
0.57
0.60
0.61
0.57
0.61
0.80

7.60
1.26
2.27
2.13
1.29
2.45
0.98

† θm-Br/θm-microbe, ratio of mobile water content of Br to that of microbes, reflecting the degree of velocity enhancement in the transport of microbes(Eq. [7]); ξBr/ξmicrobe, ratio of dispersivity of Br to that of microbes, reflecting the degree of pore-size exclusion in the transport of microbes.

www.vadosezonejournal.org · Vol. 7, No. 1, February 2008109

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ACKNOWLEDGMENTS

This study was funded by the Foundation for Research, Scienceand Technology (New Zealand) under contracts no. CO3X0303 andCO9802. We thank Dr. Scott Bradford of the U.S. Salinity Laboratory,
Riverside, CA, for his valuable comments on the manuscript.

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