Journal of Environmental Quality
TECHNICAL
REPORTS
TECHNICAL
REPORTS
WETLANDS AND AQUATIC PROCESSES
Phosphorus Retention in a Newly Constructed Wetland
Receiving Agricultural Tile Drainage Water
Pia Kynkäänniemi,* Barbro Ulén, Gunnar Torstensson, and Karin S. Tonderski
E
nhanced phosphorus (P) concentrations are a
One measure used in Sweden to mitigate eutrophication of waters
is the construction of small wetlands (free water surface wetland for
phosphorus retention [P wetlands]) to trap particulate phosphorus
(PP) transported in ditches and streams. This study evaluated P
retention dynamics in a newly constructed P wetland serving a 26-ha
agricultural catchment with clay soil. Flow-proportional composite
water samples were collected at the wetland inlet and outlet over 2
yr (2010–2011) and analyzed for total P (TP), dissolved P (DP),
particulate P (PP), and total suspended solids (TSS). Both winters
had unusually long periods of snow accumulation, and additional
time-proportional water samples were frequently collected during
snowmelt. Inflow TP and DP concentrations varied greatly (0.02–
1.09 mg L−1) during the sampling period. During snowmelt in 2010,
there was a daily oscillation in P concentration and water flow in
line with air temperature variations. Outflow P concentrations
were generally lower than inflow concentrations, with net P losses
observed only in August and December 2010. On an annual basis,
the wetland acted as a net P sink, with mean specific retention
of 69 kg TP, 17 kg DP, and 30 t TSS ha−1 yr−1, corresponding to
a reduction in losses of 0.22 kg TP ha−1 yr−1 from the agricultural
catchment. Relative retention was high (36% TP, 9% DP, and
36% TSS), indicating that small constructed wetlands (0.3% of
catchment area) can substantially reduce P loads from agricultural
clay soils with moderately undulating topography.
problem for many inland lakes and coastal areas (Smith,
1998), and losses from agricultural areas are one of the
main sources (Withers and Haygarth, 2007). In Sweden, losses
of total phosphorus (TP) from agricultural areas contribute
40% of the TP reaching the Baltic Sea (Brandt et al., 2008).
Phosphorus is one of the factors behind increased eutrophication and associated algae and cyanophyceae blooms in the
Stockholm Archipelago and the Baltic Proper (Boesch et al.,
2006). The eutrophied state of the Baltic Sea has generated much
concern, and international decisions requiring all surrounding
regions to reduce the P load have come into force (Brandt et al.,
2008). In addition, Sweden’s national environmental goals and
the EU Water Framework Directive demand improvements in
surface water quality and require a reduction in nitrogen (N) and
phosphorus (P) losses from land areas using various mitigation
measures (Swedish EPA, 2010).
One important countermeasure is to construct or restore
wetlands. Studies have documented a significant removal of N
and P in wetlands receiving urban or agricultural stormwater
(Carleton et al., 2001). Free water surface (FWS) wetlands
have also been established as nutrient sinks downstream from
agricultural hot spots, such as cattle exercise yards (Gottschall
et al., 2007) and farm yards (Dunne et al., 2005). Constructed
wetlands and buffer zones are countermeasures that qualify for
environmental subsidies in Sweden. However, there is insufficient
knowledge about the effectiveness of these wetlands and buffer
zones as sinks for P, especially in areas with clay soil that have
relatively large transports of P to surface waters (Ulén et al.,
2007). Most of the wetlands constructed in agricultural areas
of Sweden have been positioned and designed for N removal or
biodiversity and not for P retention. Free water surface wetlands
are usually designed as shallow ponds with varying amounts of
vegetation (submerged or emergent) to promote denitrification,
which is the main removal process for N (Kadlec, 1994). For P,
the main retention process is sedimentation, but P is also retained
by chemical sorption and biological uptake by plants and algae
(Reddy et al., 1999). These processes require different wetland
designs to achieve as high P retention as possible.
Copyright © American Society of Agronomy, Crop Science Society of America,
and Soil Science Society of America. 5585 Guilford Rd., Madison, WI 53711 USA.
All rights reserved. No part of this periodical may be reproduced or transmitted
in any form or by any means, electronic or mechanical, including photocopying,
recording, or any information storage and retrieval system, without permission in
writing from the publisher.
P. Kynkäänniemi, B. Ulén and G. Torstensson, Swedish Univ. of Agricultural
Sciences, Dep. of Soil and Environment, P.O. Box 7014, SE-750 07 Uppsala, Sweden;
K.S. Tonderski, Linköping Univ., IFM Biology, Se-581 83 Linköping, Sweden.
Assigned to Associate Editor Marc Stutter.
J. Environ. Qual. 42:596–605 (2013)
doi:10.2134/jeq2012.0266
Received 10 July 2012.
*Corresponding author (pia.kynkaanniemi@slu.se).
Abbreviations: Ac, upstream loading catchment area; Aw, wetland surface area;
DP, dissolved phosphorus; FWS, free water surface; P wetland, free water surface
wetland for phosphorus retention; TP, total phosphorus; TSS, total suspended solids.
596
Phosphorus removal efficiency in FWS wetlands receiving
nonpoint source runoff varies considerably due to wetland
design and location as well as annual variations in water flow
and P loading (Braskerud et al., 2005; Tonderski et al., 2005).
Hydraulic load is an important factor for nutrient retention
in wetlands (Arheimer and Wittgren, 2002; Koskiaho, 2006),
along with seasonality and the nutrient load (Richardson,
1985). In one month, a wetland may act as a P sink, whereas
in the next month it may release a corresponding amount of P.
High flow events during spring and autumn are most important
for P retention in temperate regions. During these periods, the
transport of P and particles from arable fields is large, and the
biological activity is low. During high flow events, short water
residence times reduce settling of particles with attached P and
may lead to resuspension of previously settled particles. Wetland
surface area (Aw) in relation to the upstream loading catchment
area (Ac) is therefore a determining factor for the load and thus
the wetland retention efficiency. In a certain location, a higher
Aw/Ac ratio increases the retention time of the water, allowing
more time for particles to settle and sorption to occur. This
also decreases the resuspension and loss of P already captured
in the wetland (Koskiaho, 2006), resulting in a more efficient
relative retention (in % of P load). In contrast, the area-specific
retention will be lower because there is a positive relationship
between P load and area-specific P retention (Braskerud, 2002;
Kadlec, 2005).
Other catchment characteristics influence the P loading to
wetlands. The average TP retention in seven FWS wetlands
in Sweden varying in size from 0.06 to 2.2% of the catchment
area was reported to be 3 to 58 kg TP ha−1 yr−1, which was
equivalent to 9 to 38% of the TP load (Strand and Weisner,
2013). Seventeen wetlands in Scandinavia, Switzerland, and
the United States evaluated by Braskerud et al. (2005) varied
in size from 0.007 to 8.7% of the catchment area, and the
relative retention of particulate P (PP) and dissolved P (DP)
increased with increasing wetland surface areas. In Finland, the
recommendation for wetland size relative to catchment area is 1
to 2% (Ruohtula, 1996) or >2% (Puustinen et al., 2001). In line
with this, Koskiaho (2006) found that the relatively small Alastro
FWS wetland (0.5% of the catchment area) only retained 6 kg
TP ha−1 yr−1 (7% of TP load) and acted as a source rather than
a sink of DP with −19 kg ha−1 yr−1 (−22% of TP). The author
concluded that the Aw/Ac ratio was too low for a flat watershed
dominated by clay soil, resulting in retention times that were too
short for settling of fine particles and events when resuspension
occurred. However, also in relatively large wetlands (>1%
of catchment area), considerable interannual variations in P
removal efficiencies have been observed. The annual removal was
−11 and 59% for a wetland covering 9% of the catchment area
( Jordan et al., 2003), whereas a variation from −54 to 80% was
observed by Kovacic et al. (2000) for wetlands covering 3 to 6%
of the watershed areas. Tanner et al. (2005) reported retention
efficiencies of −101% for the first year and 12% for the second
year for a wetland with a Aw/Ac ratio of 1%. Extended periods of
P release were also observed in three other wetlands, and this was
attributed to the facts that the inflowing P was predominantly in
dissolved form and the wetlands were constructed on P-rich soils
(Tanner and Sukias, 2011).
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In contrast, in Norway the trend has been to design small
wetlands (0.06–0.4% of the catchment area) focusing on the
sedimentation process, with a deeper pond for sedimentation
followed by a shallow vegetation filter. These free-water surface
wetlands for P retention (P wetlands) are reported to be efficient
traps for particles and TP (260–710 kg ha−1 yr−1 or 21–44% of
TP load) in sloping areas with silty soil (Braskerud, 2002). The
P is removed mostly as PP at rates representing up to 45% of
the load. The author attributed the high PP removal to careful
design and appropriate wetland location in streams with high
transport of particles eroded from the soils in the catchments.
It was also suggested that the location close to the source areas,
with a short transport distance to streams, may have resulted in
less destruction of the eroded clay aggregates before reaching the
wetlands. This resulted in a higher settling rate than could have
been expected for disaggregated clay particles, as later confirmed
in a study of the settled particles (Sveistrup et al., 2008). In
contrast, the retention of DP in those wetlands was only 5%
(Braskerud, 2002).
In 2010, the Swedish Board of Agriculture implemented
a new subsidy for P wetlands based on Norway’s positive
experiences. However, wetlands with the Norwegian design and
location have not been studied under Swedish conditions (i.e.,
clay soils, less undulating topography, and substantial P losses
through tile drainage systems). Studies have shown that the
runoff from drainage pipes contains up to 40% P associated with
very fine clay particles and colloids (Ulén, 2004). It is likely that
the size of the soil particles in the inflow has a substantial impact
on the efficiency of wetlands constructed as P traps. Hence, it is
important to determine the P removal that can be achieved in P
wetlands receiving loads from clay soils with tile drains.
The aim of this study was to evaluate (i) the initial 2-yr
effectiveness of a wetland designed for P retention receiving
agricultural tile drainage water from a small catchment with clay
soil and a moderate slope in Sweden and (ii) the P concentration
and retention dynamics in the wetland in different seasons.
Materials and Methods
Site Description
The Bergaholm P wetland (59°14′2.47′′ N, 17°42′44.82′′ E)
was constructed in August 2009 to reduce the P load to Lake
Bornsjön, which serves as the reserve drinking water reservoir for
the city of Stockholm, Sweden. The climate in the area is cold
temperate, with 30-yr mean annual precipitation of 576 mm
and a mean annual temperature of 6.4°C (Alexandersson et al.,
1991). The 30-yr mean period with snow cover is slightly more
than 2 mo per year (Ulén et al., 2007). The mean maximum snow
depth during winter was 0.3 m, and the maximum measured
snow depth during the reference period (1961–1990 ) was 0.6 m
(SMHI, 2012). In contrast, the winters in the study period
(2009–2010 and 2010–2011) were unusually long (3–5 mo),
with nearly permanent snow cover interrupted by just one or
two short periods of snowmelt. The small catchment area (26 ha)
consists of cultivated agricultural fields (11 ha), horse paddocks
(3 ha), and forests (12 ha). The mean animal density in the
paddocks is high (3.75 animal units ha−1) (Parvage et al., 2011).
Soil P characterization by Parvage et al. (2011) revealed high soil
P status after extraction in acid (pH 3.75) ammonium lactate
597
solution (P-AL) (Egnér et al., 1960). Topsoil
samples in some areas of the horse paddock
contain around 500 mg P-AL kg−1 soil, which
is over 80-fold higher than the median value for
Swedish arable soils (Eriksson et al., 2010). The
topsoil in the catchment typically has around
60% clay and a similar texture to an observation
field located nearby (Ulén and Persson, 1999).
Wetland Design
The 0.08-ha wetland (0.3% of the catchment
area) was constructed by opening a large drainage
pipe and diverting the water through the wetland
before discharging it into Lake Bornsjön at the
original pipe outlet (Fig. 1). The wetland was Fig. 1. Aerial views of the catchment area (left) and the Bergaholm free-water surface
designed to fit into the landscape and has a long, wetland for phosphorus retention (P wetland) to the right. Flow proportional sampling at
narrow shape to increase hydraulic efficiency. the inlet (FPin) and outlet (FPout).
This narrow shape in combination with a deep
outflow was recalculated and set as equal to the inflow when the
inlet pond makes maintenance easier, facilitating future removal
outlet water level was above 135 mm.
of P-containing sediment, which can then be returned to the
The pattern of groundwater movement was determined
fields. The wetland is designed to specifically retain particles and
by measuring the pressure level in 12 piezometers placed in
associated P. Thus, the inlet comprises a 1-m-deep and 27-m-long
pairs around the wetland. The piezometers were closed at the
pond (0.02 ha) intended to decrease the water velocity and thus
bottom, and in each pair one piezometer had an inlet slot at
to allow particles and associated P to settle. The pond is followed
0.4 m and the other an inlet slot at 0.8 m below the soil surface
by two 0.3-m-deep vegetated areas (0.03 ha each) with a total
to assess whether groundwater was mainly moving upward or
length of 73 m. Their intended function is to act as filters for
downward. Groundwater level was determined by lowering and
particles and to protect trapped sediments from resuspension
simultaneously blowing into a graded long tube and listening for
by stabilizing them within plant roots. To prevent erosion,
the sound of bubbles, which indicated the groundwater level.
the edges of the P wetland are covered with a coarse-meshed
Water Sampling and Analysis
coconut fiber net and sown with a mixture of meadow grasses
and herbs. A few meters west of the wetland, a long open ditch
Flow-proportional composite samples were collected at
has been constructed to prevent water from this small uphill
the wetland inlet and outlet (Fig. 1) weekly or biweekly year
catchment area entering the P wetland and to ensure that the
round. After 20,000 L of water had passed through the wetland,
water flow measured at the pipe inlet represents the total inflow
the data logger triggered a peristaltic pump that transported
to the wetland. To speed up the establishment of vegetation,
approximately 20 mL of subsample to a 20-L glass bottle placed
locally growing macrophytes (greater pond sedge [Carex riparia
in a refrigerator. Samples were collected on 54 occasions during
Curtis], yellow iris [Iris pseudacorus L.], simplestem bur-reed
the 2 yr of sampling: 30 samples were collected in 2010, and 24
[Sparganium erectum L.], and purple loosestrife [Lythrum
samples were collected in 2011. Heating cables prevented pumps
salicaria L.]) were planted in the shallow areas in September
and tubes from freezing and enabled sampling to be performed
2009. Vegetation density increased during the study period, and
year round. During critical periods triggered by snowmelt, the
new species colonized naturally. Filamentous algae blooms were
dynamics of water quality changes were investigated using timeobserved in the summers of both years.
composite samples collected simultaneously at the inlet and
outlet. Three hourly samples composed of one subsample per
Water Flow and Groundwater Measurements
30 min were collected with one ISCO GLS continuous sampler
For the purposes of this study, the wetland inlet and outlet
placed at the inlet and one at the outlet.
were equipped with V-notch weirs, load cells (Scaime), and a
Water samples were analyzed according to the European
trunk for water displacement connected to a Campbell CR1000
Committee for Standardization (ECS, 1996). Total P was
datalogger (Campbell Scientific, Inc.) to register the average
determined as soluble molybdate-reactive P after acid oxidation
water level every hour. During two periods in April and May
with K2S2O8. Dissolved phosphorus was determined after
2010, technical problems occurred, and water flow data were
prefiltration using filters with a pore diameter of 0.2 μm
missing. For those periods, the water flow was estimated using
(Schleicher & Schüll GmbH). The difference between TP in
manual measurements of water levels at the V-notch weirs,
nonfiltered and filtered water was considered to be PP. Total
and the water flow dynamics were obtained from continuous
suspended solids (TSS) were determined as the weight difference
water flow measurements in the nearby observation field. In
before and after filtration with the same type of filters.
periods when outflow data alone were missing, the outflow
Data Analyses and Statistics
was calculated based on regression analysis of measured inflow
and outflow as 93% of the inflow. A fault in the design of the
Mean water residence time was calculated by dividing the
outlet V-notch weir caused measurement errors in periods with
volume of the wetland (m3) by the daily water inflow (m3 d−1).
very high outflow. To avoid overestimation of the retention, the
598
Journal of Environmental Quality
Hydraulic load (m yr−1) was calculated by dividing the
cumulative annual inflow (m3) by the area of the wetland
(m2). Loads of P and TSS (kg) to the wetland and
transport from the wetland were calculated by multiplying
the concentration (mg L−1) in each composite sample at
the inlet by the total volume of water (m3) entering the
wetland during the corresponding sampling period and
the concentration in the outlet sample by the outlet water
volume, respectively. Specific retention (kg ha−1) was
calculated by subtracting the nutrient transport out of the
wetland from the nutrient load. Relative retention (%) was
estimated by dividing the amount of nutrient retained by
the nutrient load. Any relationships observed between P
concentrations in time-proportional water samples during
snowmelt 2010 and the corresponding water flow for
the same period were indicated by Pearson correlation.
The relationship between TP retention and inflow, air
temperature, PP, DP, and TSS concentrations was further
analyzed using a multiple linear regression model with
auto-regressive errors, with two lags for the high-frequency Fig. 2. Precipitation (black bars), air temperature (gray line), and snow depth
time-composite samples from snowmelt in 2010. The time (gray area) during the 2-yr experimental period measured at the nearby
lags were chosen to match the frequency of every sample (3 Swedish meteorological climate station in Södertälje.
h) and every second sample (6 h). These statistical analyses
smaller than 0.3% and are located in regions with higher annual
were performed using SAS 9.2 software. To determine whether
runoff. In Norway, P wetlands receive much higher loads (241–
the mean TP concentration in the inflow was significantly
661 m yr−1) (Braskerud, 2002), whereas the hydraulic loads on
different from that in the outflow, the method proposed by
wetlands in agricultural areas in Finland are lower (7–47 m yr−1)
Zwiers and von Storch (1995) was used. This method is based
(Koskiaho et al., 2003).
on computation of the effective sample size (i.e., the sample
The outflow for the entire study period (including periods with
size adjusted by taking the magnitude of serial correlation into
estimated water flow when data were missing) was 88% of the
account). This is then used in the formula of the t test, and the
inflow. The pattern of pressure levels in the piezometers indicated
test statistics are compared with table values given in the article
that water from the wetland infiltrated to the groundwater year
by Zwiers and von Storch (1995). This method was used because
round, which may explain part of this difference. The infiltration
the observations we had were serially correlated in time and thus
seems reasonable because the wetland is located just upstream of
could not be counted as “full” observations.
a big lake, which means that there is a hydraulic gradient toward
the lake.
Results and Discussion
Water Load
Water Quality Dynamics
The water inflow to the P wetland during the study period
(15 Jan. 2010 to 31 Dec. 2011) was highly variable with several
extreme peaks (Fig. 3a), resulting in daily water residence times
ranging from 5 h to 1010 d during extreme low flows in summer
(median 7 d). The winters of 2009–2010 and 2010–2011 were
cold, with snow cover up to 0.5 m deep (Fig. 2). This resulted
in intense snowmelt periods in March each year (Fig. 3a).
There was also a short snowmelt in January 2011. When these
snowmelts occurred, the wetland received the highest daily
inflow of the entire study period. In 2011, the winter was mild
until 31 December and had only 0.02 m of snow cover for a few
days in the middle of December. In summer 2010, two extremely
intensive periods of rainfall within 5 d at the end of July resulted
in the highest hourly inflow (248 m3 h−1) (Fig. 2). The intensive
rain was followed by a rainy August, which resulted in a generally
high flow for that month. The average annual hydraulic load was
60 m yr−1, which was low in comparison with that reported for
seven other monitored wetlands constructed in agricultural areas
in Sweden (range, 7–725 m yr−1; median, 128 m yr−1) (Strand
and Weisner, 2013). That dataset covers wetlands that vary
in size from 0.06 to 2.2% of the catchment area, but most are
Phosphorus Dynamics Based on Flow-Proportional Sampling
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Phosphorus concentrations in the inflow varied greatly
during the 2 yr of sampling (Fig. 3b, c). The average inflow
concentrations of 0.30 TP mg L−1 and 0.10 mg DP L−1 showed
that about 67% of the P was bound to particles, which was
confirmed by the high TSS concentrations (Table 1). However,
this varied considerably from 22 to 95%. Mean TP concentrations
in the outlet were significantly lower than in the inlet (0.18 mg
TP L−1). The p value of the test for different mean concentrations
cannot be determined exactly but was approximated to be 0.05
by interpolation between the sample sizes given in the table in
(Zwiers and von Storch, 1995). The DP concentration was lower,
but not significantly so, at 0.06 mg DP L−1. Particulate P also
dominated in the outflow water, with a TSS concentration of
87 mg L−1. The highest inflow concentrations of TP (1.09 mg L−1)
and DP (0.51 mg L−1) were observed in October 2010 (Fig. 3b,
c), whereas the highest inflow TSS concentration (488 mg L−1)
was observed during the short snowmelt period in January
2011 (Fig. 3d). The highest TP concentration in the outflow
(0.47 mg L−1) occurred in November 2011, the highest outflow
DP concentration (0.22 mg L−1) occurred in July 2010 after
599
Fig. 3. (a) Inflow of water to the wetland (m3 d−1) during the sampling period. Incoming (black) and outgoing (white) concentrations (mg L−1) in
flow-proportional composite water samples of (b) total phosphorus (TP), (c) dissolved phosphorus (DP), and (d) total suspended solids (TSS).
Circles indicate where inflow concentrations were lower than outflow concentrations.
the intensive rainfall event, and the highest TSS concentration
(568 mg L−1) occurred in September 2011. Although the outflow
TP, DP, and TSS concentrations were usually lower than those in
the inflow, there were a few short-term exceptions. During both
snowmelt events in March, when the water flow was large, the
concentrations of TP and TSS in the outflow were slightly higher
than in the inflow (Fig. 2). On 25 Mar. 2011, we had to shovel
out the sediment that had accumulated in the inlet well. The
Table 1. Hydraulic load, mean total phosphorus, and dissolved phosphorus concentrations in the inlet and outlet. Load of total phosphorus
and total suspended solids, area-specific and relative retention of total phosphorus, dissolved phosphorus, particulate phosphorus, and total
suspended solids. All values based on flow-proportional composite water samples taken in the Bergaholm wetland during the period 15 Jan. 2010
to 31 Dec. 2011.
Year
2010
2011
Average
Hydraulic
load
Mean concentration†
TP
DP
Inlet
Outlet
Inlet
Outlet
TP
Load
Retention
m yr−1
53
67
60
————— mg L−1 —————
0.25
0.17
0.10
0.06
0.36
0.20
0.10
0.06
0.30
0.18
0.10
0.06
—————————————————— kg ha−1 yr−1 ——————————————————
192 70,417
54
(28)‡
20 (10)
24
(12)
22,048
(31)
194 95,170
84
(43)
15 (8)
68
(35)
36,985
(39)
193 83,036
69
(36)
17 (9)
46
(24)
29,663
(36)
TSS
TP
DP
PP
TSS
† DP, dissolved phosphorus; PP, particulate phosphorus; TP, total phosphorus; TSS, total suspended solids.
‡ Values in parentheses are relative retentions in percent of the loads.
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Journal of Environmental Quality
Fig. 4. (a) Inflow (m3 h−1) and air temperature (°C), (b) total phosphorus (TP), and (c) total suspended solids (TSS) concentrations (mg L−1) in timeproportional water samples on four sampling occasions during snowmelt in 2010.
large amount of sediment carried to the wetland during the high
flow event was probably unable to settle before emptying and was
instead transported out of the wetland, which could have caused
the higher outflow concentrations seen at the beginning of April.
The inlet well was emptied once more on 19 Oct. 2011, which
again might have caused enhanced outflow TSS concentrations.
In August 2010, after the heavy rainfall at the end of July, DP was
higher in the outflow, which could have been caused by flush-out
of algae cells and filaments because the wetland was covered with
filamentous green algae. During ice cover periods in December
2010, TP and DP outflow concentrations were also higher than
the inflow concentrations. A possible reason for this could be
that the long period with ice cover caused anoxia that reduced
iron in the wetland sediment, which released the P bound to
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iron. Similar observations were made in another Swedish FWS
wetland, where it was suggested that accumulated litter and
organic sediment caused the development of anoxic conditions,
with the subsequent release of iron-bound P during ice cover
periods ( Johannesson et al., 2011).
Phosphorus Dynamics Based on High-Frequency
Time-Proportional Sampling
High-frequency time-proportional sampling during the
2010 snowmelt revealed a daily oscillation in TP and TSS
concentrations and water flow, which followed variations in air
temperature (Fig. 4). There was a delay of some hours between
the peak concentrations in the inflow and outflow for TP and
TSS. The variation within a single day was considerable; over an
18-h period, the TP concentration sometimes varied by more
601
than a factor of 2 and the TSS concentration by a factor of 4. The
peak in the inflow concentration occurred in the initial phase
of the flow peak increase (0.69) (Table 2). Water residence time
was 3 to 9 h for the first two periods of sampling and 6 to 16 h
for the third. Even though the water flow and water retention
time were short, there was a decrease in the concentrations of TP
and TSS in the outflow, and the retention of TP, DP, and TSS
correlated significantly with the inflow concentrations (Table 2).
General linear model analysis showed that the TP retention was
positively correlated with inflow and temperature but also with
P concentrations (Table 3). The residuals from the autoregressive
model were normally distributed. Total suspended solids and PP
were strongly correlated; hence, TSS was not included in the
model to avoid multicollinearity. This shows that the wetland
also functioned as a P trap in periods with simultaneous high
flow and high concentrations. The peak flow (137 m3 h−1) on 1
Apr. 2010 was not covered by this intensive sampling period due
to an interruption in the sampling. Calculations based on the
flow-proportional sampling (weekly or fortnightly) showed a net
release of TP on that date, which indicates that there might be a
water flow threshold (>130 m3 h−1) above which the Bergaholm
wetland did not function as a sink for particles and P. An extreme
episode reported for one of the Norwegian wetlands had a flow
peak of 4428 m3 h−1 (Braskerud, 2001). This Norwegian wetland
had a hydraulic load over 10-fold higher than Bergaholm
wetland, larger particles in the inflow, and a settling rate similar
to silt particles (Sveistrup et al., 2008). This is a likely explanation
for the apparent difference between the wetlands regarding water
velocity when flush-out of sediment occurred.
The delay between the inlet and outlet and the hourly
concentration variations emphasize how important the sampling
method is for retention estimates. In wetlands with dynamic
water flow and concentration changes similar to those in the
Bergaholm wetland, it is important to have flow-proportional
sampling with water flow measurements at the inlet and outlet
for more reliable estimates of retention.
Phosphorus Load and Retention
In total, 0.6 kg TP ha−1 yr−1 and 267 kg TSS ha−1 yr−1 leached
from the arable land and horse paddocks in the 26-ha catchment
studied here. This is high for Swedish conditions, where the
average TP loss is 0.4 kg ha−1 yr−1 (Ulén et al., 2007). Clay soils
such as that in this study normally have higher P losses than
average and are prone to erosion. In combination with long-term
fertilization with manure and the fact that parts of the horse
paddock had an extremely high soil P status and a high degree of
P saturation (Parvage et al., 2011), this classifies the catchment
Table 2. Pearson correlation coefficients between water flow or total
phosphorus retention (time-proportional sampling) and the inflow
concentrations of total phosphorus, particulate phosphorus, dissolved
phosphorus, and total suspended solids during snowmelt 2010 (82
observations).
TP
Inflow, m3 h−1
TP retention, kg
Inflow concentration†
PP
DP
TSS
————————— mg L−1 —————————
0.69
0.63
0.60
0.58
0.69
0.62
0.48
0.58
† DP, dissolved phosphorus; TP, total phosphorus; TP, total phosphorus;
TSS, total suspended solids.
602
as a “hot-spot” for P losses. The load to the wetland was 193 kg
TP ha−1 yr−1 and 83 t TSS ha−1 yr−1 (Table 1), which was more
than two times higher than most TP loads reported in the
literature for other wetlands receiving runoff from agricultural
land (Higgins et al., 1993; Kovacic et al., 2000; Jordan et al.,
2003; Koskiaho et al., 2003; Reinhardt et al., 2005; Tanner et
al., 2005). However, three of the wetlands with low Aw/Ac ratios
in the study by Strand and Weisner (2013) received loads that
were comparable (i.e., in the 100–200 kg ha−1 yr−1 range). The
two Swedish FWS wetlands with higher P loads (400–675 kg
ha−1 yr−1) had a >7-fold higher hydraulic load but had a lower
TP inflow concentration (0.06–0.16 mg L−1). Higher hydraulic
loads were also the main reason for the up to 10-fold higher TP
loads on the Norwegian P wetlands (i.e., 970–1910 kg ha−1 yr−1)
(Braskerud, 2002).
The Bergaholm wetland was a net P and TSS sink on an
annual basis, retaining 69 and 29,700 kg ha−1 yr−1, respectively
(Table 1), which corresponded to an annual retention of 0.22 kg
TP ha−1 catchment area. This was much higher than reported in
the cited studies of wetlands receiving lower loads (see above),
which could be expected because the P load is an important
determining factor for the retention. However, the retention was
also two times higher than reported from three Swedish wetlands
with similar loads and was in the same range as reported for
two wetlands with two to three times higher P load Strand and
Weisner (2013). In addition, the study period covered the first
2 yr after construction of the wetland, when the bottom surface
had not stabilized (i.e., there was probably more erosion from
the bottom sediment and edges because the vegetation had not
completely established). In the second year, the loads of TP and
particles were larger and the retention also higher, suggesting that
even higher retention might be achieved in the next few years
(Table 1). Considering that the study period covered 2 yr with
extreme snowmelts, resulting in very low residence times in the
wetland, the P retention would probably be higher during more
normal winters. Nevertheless, the P wetland retained P quite
well, suggesting that the design might be efficient for trapping
TP in flat catchments with tile-drained clay soils. On the other
hand, the area-specific TP retention in small P wetlands in
Norway was even higher (260–720 kg ha−1 yr−1), probably due
Table 3. Results from a multiple linear regression model with
autoregressive errors for the relationship between total phosphorus
retention and water flow, inflow concentrations (time-proportional
sampling) of dissolved phosphorus, particulate phosphorus, and air
temperature during snowmelt 2010.
Variables†
Estimate
Intercept
Inflow, m3 h−1
DP, mg L−1
PP, mg L−1
−0.021***
−0.0002***
0.130***
0.184***
0.0004**
0.722
0.797
82
Air temperature, °C
Regress R2
Total R2
No. observations
SE
0.002
0.00003
0.019
0.020
0.0002
** Significant at the 0.01 probability level.
*** Significant at the 0.001 probability level.
† DP, dissolved phosphorus; PP, particulate phosphorus.
Journal of Environmental Quality
ton ha−1 mo−1) (Fig. 5b). Accumulated sediment was shoveled
out of the inlet well in March and at the end of October 2011,
which could have contributed to the negative TSS retention in
March and November.
As expected, some of the variation in monthly TP retention
was explained by the load variation (Fig. 6). This correlation
between area-specific P load and retention generally applies to
nutrient removal in treatment wetlands (Braskerud et al., 2005;
Kadlec, 2005). However, both extreme flow events and seasonal
changes in the biogeochemical conditions of the wetland
contributed to the occasionally large deviations from this general
relationship.
In contrast to the positive relationship between areaspecific load and retention, the relative retention (% of load) is
negatively correlated with the load (Braskerud et al., 2005). The
Bergaholm P wetland retained 36% of incoming TP and TSS
(Table 1), which was higher than for three of the five Norwegian
P wetlands (21–44%) mentioned earlier with much higher loads
(Braskerud, 2002). However, it was higher than that observed in
most previously studied Swedish (10–38%), Finnish (7–62%),
Swiss (23%), U.S. (23–88%), and New Zealand (12%) FWS
wetlands with lower loads (Higgins et al.,
1993; Kovacic et al., 2000; Jordan et al.,
2003; Koskiaho et al., 2003; Reinhardt
et al., 2005; Tanner et al., 2005; Strand
and Weisner, 2013). Two exceptions with
62 and 88% mean annual efficiency were
wetlands with large Aw/Ac ratios (5 and
9%) and high inflow TP concentrations
(Higgins et al., 1993; Koskiaho et al.,
2003). This indicates that the design of
the Bergaholm P wetland facilitated P
removal. However, the Alastro wetland
in Finland has a similar design (0.5% of
the catchment area and a deeper pond
followed by a shallow vegetation area)
but lower retention efficiency (7%). A
possible explanation is the lower length
to width ratio of 5 in the Alastro wetland,
compared with 14 in the Bergaholm
P wetland, which may have impaired
its hydraulic efficiency (Persson and
Wittgren, 2003).
The first-order removal rate constant
k (m yr−1) can be used to compare the
efficiency of P retention in different
wetlands
while
accounting
for
differences in hydraulic load and inflow
concentrations (Kadlec and Knight,
1996). Braskerud et al. (2005) suggested
that k can be used as an approximation of
the P settling velocity but also showed that
the k value depends on the hydraulic load.
However, if the hydraulic load is similar,
then the k value can be used to compare
the P retention efficiency between
wetlands. In the Bergaholm P wetland, k
−1
−1
Fig. 5. Monthly area-specific (kg or t ha wetland area yr ) retention in gray bars. Diamonds show
was 30, which was higher than in all the
relative retention (%) and black line hydraulic load (m mo−1). (a) Total phosphorus (TP). (b) Total
wetlands in Finland, Switzerland, and
suspended solids (TSS).
to a higher P load and different soil properties, as discussed above
(Braskerud, 2002; Sveistrup et al., 2008).
There were large variations in monthly area-specific TP
retention (range, −0.8 to 36.6 kg TP ha−1 yr−1), with low
retention in the summer season and high retention in the
autumn (Fig. 5a). The winter and spring seasons varied between
the 2 yr. In 2009–2010, P retention was very low during the
cold winter with low flow and high in the spring of 2010 with
the extreme snowmelt. In 2011, the short snowmelt period in
January resulted in a high load of PP and a high P retention. In
March, the P load was only half the P load in January, and the
PP fraction in the inflow was smaller. In combination with a
higher hydraulic load in March, this resulted in lower P retention
in March than in January. Higher outflow P concentrations
during short periods of the year, such as during snowmelt, did
not usually result in a net monthly loss of TP. There were two
exceptions when a monthly loss of TP was observed: in August
2010, with intensive rainfall, and in December 2010, with a low
flow when anoxic conditions might have resulted in a release of
P. However, a minor release of TSS was observed in March, May,
and November 2011 and much more in September 2011 (2.8
www.agronomy.org • www.crops.org • www.soils.org
603
the United States evaluated by Braskerud et al. (2005), which
had a hydraulic load below 124 m yr−1. This further supports
the conclusion that the design of the Bergaholm wetland was
favorable for high PP removal.
The relative retention of PP increased in the second year
from 12 to 35%. The period is not enough to evaluate for how
long the P wetland might retain P. Thirty tons of sediment
were captured over 2 yr, which implies that the first pond
would be half filled after 7 yr and the sediment would have to
be removed. However, for the filtering aspect the function may
improve when the vegetation has fully established, which may
contribute to increased filtration and sedimentation capacities
and reduced resuspension and transport of particles from the
bottom and edges (Braskerud, 2001). Settled particles have to
be removed at regular, but as yet unknown, intervals to prevent
flush-out during extreme peak flows. Consequently, more longterm monitoring of the wetland function is needed to get a
better qualitative understanding of how settling rates depend on
catchment characteristics. This would also serve as valuable input
for developing design guidelines (e.g., how large wetlands need
to be for a certain catchment type).
The effectiveness of retained P is often strongly related to the
form of P entering the wetland (i.e., more PP than DP is generally
retained) (Hoffmann et al., 2009). Unusually high dissolved
P soil concentrations in the horse paddocks in the catchment
(Parvage et al., 2011) and a clay soil with the main mineral
component illite (Ulén and Snäll, 2007) contributed to a high
concentration of DP in the drainage water. However, DP was
also retained in the Bergaholm wetland, although at a relatively
lower rate than for PP (9 versus 24% of the TP load) (Table 1).
Over the 2 yr of the study, 28% of the DP load was retained in
the wetland. This agrees with observations from other FWS and
P wetlands (Braskerud et al., 2005), although contradictory
observations have also been reported. For example, Tanner and
Sukias (2011) reported poor P removal in three constructed
wetlands receiving tile drain water with predominantly dissolved
P. Over a 3- to 5-yr period, all those wetlands were net sources of
P. In Bergaholm, one period with release of DP occurred after the
intensive rain in the summer of 2010, which was followed by an
outflow concentration of 0.22 mg DP L−1. The general summer
outflow concentrations were below 0.05 mg L−1, resulting in a
low transport of bioavailable P to the lake in this season. Because
summer is the most sensitive period for lake water quality, this
was a favorable effect of the wetland. Because removal of the
settled sediment is necessary to maintain the wetland function as
a trap for particulate P, this might also help sustain the sorption
capacity for dissolved P. Further investigations are necessary to
identify the linkage between settling of inflowing particles and
sorption of dissolved P.
Conclusions
This study evaluated the initial 2-yr effectiveness of a small
wetland designed for retention of the P in agricultural subsurface
drainage water. The results showed that this first Swedish P
wetland effectively retained TP and TSS (69 kg ha−1 yr−1 and
30 t ha−1 yr−1, corresponding to 36% of the loads). This suggests
that P wetlands designed for trapping particulate P and located
close to the source can substantially reduce P loadings from
604
Fig. 6. Relationship between monthly phosphorus (P) load (kg ha−1
mo−1) and area-specific P retention (kg ha−1 mo−1).
Swedish agricultural clay soil areas with moderately undulating
topography.
The time delay between the flow increase in the inlet and in
the outlet and the hourly variation in concentrations emphasize
the need for flow-proportional or extremely frequent water
sampling for reliable retention estimates. It is also important to
conduct water flow measurements at the inlet and outlet.
Occasions where P concentrations were higher in outflow
than inflow coincided with extreme flow events or periods
with low flow and ice cover, but a net monthly loss of TP
was observed only rarely. However, the occasional flushout of sediments during high-flow events suggests that a
sediment removal scheme may be a necessary part of wetland
management. Results from longer-term studies may help to
define suitable removal intervals.
Acknowledgments
This project was financed by the Swedish Farmers’ Foundation
(SLF), with additional funding from the Swedish Environmental
Agency (Marine Environment Grant) and the Swedish University of
Agricultural Sciences. The authors thank Stockholm Water AB for
giving us the opportunity to construct this wetland and especially Johan
Frank for technical assistance and water sampling, Jonas Andersson
of WRS Uppsala AB for the technical design of the wetland, Jonas
Engkvist of Torparens Entreprenad AB for constructing the wetland,
Bengt Norén of In Situ Instruments AB for installing the logger, and
Claudia von Brömssen of the Swedish University of Agricultural
Sciences for statistical help.
References
Alexandersson, H., C. Karlström, and S. Larsson-McCann. 1991. Temperature
and precipitation in Sweden 1961–1990. Reference normals. (In Swedish.)
The Swedish Meteorological and Hydrological Institute (SMHI),
Norrköping.
Arheimer, B., and H.B. Wittgren. 2002. Modelling nitrogen removal in potential
wetlands at the catchment scale. Ecol. Eng. 19:63–80. doi:10.1016/
S0925-8574(02)00034-4
Boesch, D., R. Hechy, C. O’Melia, D. Schindler, and S. Seitzinger. 2006.
Eutrophication of Swedish Seas. Rep. 5509. Swedish Environmental
Protection Agency, Stockholm.
Brandt, M., H. Ejhed, and L. Rapp. 2008. Nutrient loads to the Swedish marine
environment in 2006. (In Swedish with English abstract.) Rep. 5815.
Swedish Environmental Protection Agency, Stockholm.
Braskerud, B.C. 2001. The influence of vegetation on sedimentation and
resuspension of soil particles in small constructed wetlands. J. Environ.
Qual. 30:1447–1457. doi:10.2134/jeq2001.3041447x
Braskerud, B.C. 2002. Factors affecting phosphorus retention in small
constructed wetlands treating agricultural non-point source pollution.
Ecol. Eng. 19:41–61. doi:10.1016/S0925-8574(02)00014-9
Journal of Environmental Quality
Braskerud, B.C., K.S. Tonderski, B. Wedding, R. Bakke, A.G.B. Blankenberg, B.
Ulén, and J. Koskiaho. 2005. Can constructed wetlands reduce the diffuse
phosphorus loads to eutrophic water in cold temperate regions? J. Environ.
Qual. 34:2145–2155. doi:10.2134/jeq2004.0466
Carleton, J.N., T.J. Grizzard, A.N. Godrej, and H.E. Post. 2001. Factors affecting
the performance of stormwater treatment wetlands. Water Res. 35:1552–
1562. doi:10.1016/S0043-1354(00)00416-4
Dunne, E.J., N. Culleton, G. O’Donovan, R. Harrington, and A.E. Olsen. 2005.
An integrated constructed wetland to treat contaminants and nutrients
from dairy farmyard dirty water. Ecol. Eng. 24:219–234. doi:10.1016/j.
ecoleng.2004.11.010
ECS. 1996. Water quality: Determination of phosphorus. Ammoniummolybdate spectrometric method, European Standards EN 1189.
European Committee for Standardization, Brussels, Belgium.
Egnér, H., H. Riehm, and W. Domingo. 1960. Untersuchungen über
die chemische Bodenanalyse als Grundlage fürdie Beurteiling des
Nährstoffzustandes der Böden: II.Chemische Extractionsmethoden
zur Phosphor und Kaliumbestimmung. Kungliga Lantbrukshögskolans
Annaler 26:199–215.
Eriksson, J., L. Mattson, and M. Söderström. 2010. Current status of Swedish
arable soils and cereal crops: Data from the period 2001–2007. (In Swedish
with English abstract.) Rep. 6349. Swedish Environmental Protection
Agency, Stockholm.
Gottschall, N., C. Boutin, A. Crolla, C. Kinsley, and P. Champagne. 2007. The
role of plants in the removal of nutrients at a constructed wetland treating
agricultural (dairy) waste water, Ontario, Canada. Ecol. Eng. 29:154–163.
doi:10.1016/j.ecoleng.2006.06.004
Higgins, M.J., C.A. Rock, R. Bouchard, and B. Wengrezynek. 1993. Controlling
agricultural runoff by use of constructed wetlands. In: G.A. Moshiri,
editor, Constructed wetlands for water quality improvement. Lewis Publ.,
Boca Raton, FL. p. 359–367.
Hoffmann, C.C., C. Kjaergaard, J. Uusi-Kämppä, H.C.B. Hansen, and B.
Kronvang. 2009. Phosphorus retention in riparian buffers: Review of their
efficiency. J. Environ. Qual. 38:1942–1955.
Johannesson, K.M., J.L. Andersson, and K.S. Tonderski. 2011. Efficiency of a
constructed wetland for retention of sediment-associated phosphorus.
Hydrobiologia 674:179–190. doi:10.1007/s10750-011-0728-y
Jordan, T.E., D.F. Whigham, K.H. Hofmockel, and M.A. Pittek. 2003. Nutrient
and sediment removal by a restored wetland receiving agricultural runoff. J.
Environ. Qual. 32:1534–1547. doi:10.2134/jeq2003.1534
Kadlec, R.H. 1994. Wetlands for water polishing: Free water surface wetlands.
In: W.J. Mitsch, editor, Global wetlands: Old and new. Elsevier Science
BV, Amsterdam.
Kadlec, R.H., and R. Knight. 1996. Treatment wetlands. CRC Press/Lewis
Publishers, Boca Raton, FL.
Kadlec, R.H. 2005. Phosphorus removal in emergent free surface wetlands. J.
Environ. Sci. Health A Tox Hazard Subst Environ Eng. 40:1293–1306.
Koskiaho, J. 2006. Retention performance and hydraulic design of constructed
wetlands treating runoff waters from arable land. Ph.D. thesis. Oulu Univ.,
Oulu, Finland.
Koskiaho, J., P. Ekholm, M. Raty, J. Riihimäki, and M. Puustinen. 2003. Retaining
agricultural nutrients in constructed wetlands: Experiences under boreal
conditions. Ecol. Eng. 20:89–103. doi:10.1016/S0925-8574(03)00006-5
Kovacic, D.A., M.B. David, L.E. Gentry, K.M. Starks, and R.A. Cooke. 2000.
Effectiveness of constructed wetlands in reducing nitrogen and phosphorus
export from agricultural tile drainage. J. Environ. Qual. 29:1262–1274.
doi:10.2134/jeq2000.00472425002900040033x
Parvage, M.M., H. Kirchman, P. Kynkäänniemi, and B. Ulén. 2011. Impact
of horse grazing and feeding on phosphorus concentrations in soil and
drainage water. Soil Use Manage. 27:367–375.
Persson, J., and H.B. Wittgren. 2003. How hydrological and hydraulic conditions
affect performance of ponds. Ecol. Eng. 21:259–269. doi:10.1016/j.
ecoleng.2003.12.004
www.agronomy.org • www.crops.org • www.soils.org
Puustinen, M., J. Koskiaho, V. Gran, J. Jormola, T. Maijala, and M. Mikkola-Roos.
2001. Constructed wetlands for agricultural water protection. Final report
of the VESIKOT-project. (In Finnish with English abstract.) The Finnish
Environment 499. Finnish Environment Institute, Helsinki, Finland.
Reddy, K.R., R.H. Kadlec, E. Flaig, and P.M. Gale. 1999. Phosphorus retention
in streams and wetlands: A review. Crit. Rev. Environ. Sci. Technol. 29:83–
146. doi:10.1080/10643389991259182
Reinhardt, M., R. Gachter, B. Wehrli, and B. Muller. 2005. Phosphorus retention
in small constructed wetlands treating agricultural drainage water. J.
Environ. Qual. 34:1251–1259. doi:10.2134/jeq2004.0325
Richardson, C.J. 1985. Mechanisms controlling phosphorus retention
capacity in fresh-water wetlands. Science 228:1424–1427. doi:10.1126/
science.228.4706.1424
Ruohtula, J. 1996. Planning of constructed wetlands and sedimentation basins.
(In Finnish.) Mimeograph series of the Finnish Environment Institute 11.
Finnish Environment Institute, Helsinki, Finland.
SMHI. 2012. Swedish Meterological and Hydrological Institute. www.smhi.se/
klimatdata/meteorologi/sno (accessed 24 Oct. 2012).
Smith, V.H. 1998. Cuktural eutrophication of inland estuarien and coastal
waters In: M.L. Pace and P.M. Groffman, editors, Successes limitations and
frontiers in ecosystem science. Springer, New York. p. 7–49.
Strand, J., and S.E.B. Weisner. 2013. Combating eutrophication of the sea and
enhancing biodiversity of the agricultural landscape: Experiences from
wetland creation in Sweden. Ecol. Eng. (in press).
Sveistrup, T.E., V. Marcelino, and B.C. Braskerud. 2008. Aggregates explain the
high clay retention of small constructed wetlands: A micromorphological
study. Boreal Environ. Res. 13:275–284.
Swedish EPA. 2010. Sweden’s environmental objectives. www.miljomal.
se/Environmental- Objectives-Portal/Undre-meny/About-theEnvironmental-Objectives/7-Zero-Eutrophication/ (accessed 6 July
2012).
Tanner, C.C., M.L. Nguyen, and J.P.S. Sukias. 2005. Nutrient removal by a
constructed wetland treating subsurface drainage from grazed dairy pasture.
Agric. Ecosyst. Environ. 105:145–162. doi:10.1016/j.agee.2004.05.008
Tanner, C.C., and J.P.S. Sukias. 2011. Multiyear nutrient removal performance
of three constructed wetlands intercepting tile drain flows from grazed
pastures. J. Environ. Qual. 40:620–633. doi:10.2134/jeq2009.0470
Tonderski, K.S., B. Arheimer, and C.B. Pers. 2005. Modeling the impact of
potential wetlands on phosphorus retention in a Swedish catchment.
Ambio 34:544–551.
Ulén, B., and K. Persson. 1999. Field-scale phosphorus losses from a drained
clay soil in Sweden. Hydrol. Processes 13:2801–2812. doi:10.1002/
(SICI)1099-1085(19991215)13:17<2801::AID-HYP900>3.0.CO;2-G
Ulén, B. 2004. Size and settling velocities of phosphorus-containing particles
in water from agricultural drains. Water Air Soil Pollut. 157:331–343.
doi:10.1023/B:WATE.0000038906.18517.e2
Ulén, B., M. Bechmann, J. Fölster, H.P. Jarvie, and H. Tunney. 2007. Agriculture
as a phosphorus source for eutrophication in the north-west European
countries, Norway, Sweden, United Kingdom and Ireland: A review. Soil
Use Manage. 23:5–15. doi:10.1111/j.1475-2743.2007.00115.x
Ulén, N., and S. Snäll. 2007. Forms and retention of phosphorus in an illite clay
soil profile with a history of fertilization with pig manure and mineral
fertilisers. Geoderma 137:455–465. doi:10.1016/j.geoderma.2006.10.003
Withers, P.J.A., and P.M. Haygarth. 2007. Agriculture, phosphorus and
eutrophication: A European perspective. Soil Use Manage. 23:1–4.
doi:10.1111/j.1475-2743.2007.00116.x
Zwiers, F.W., and H. von Storch. 1995. Taking serial correlation
into account in tests of the mean. J. Clim. 8:336–351.
doi:10.1175/1520-0442(1995)008<0336:TSCIAI>2.0.CO;2
605