Nitrous Oxide and Dinitrogen: The Missing Flux in Nitrogen Budgets
of Forested Catchments?Nitrous Oxide and Dinitrogen: The Missing
Flux in Nitrogen Budgets of Forested Catchments? Eric M. Enanga,†
Nora J. Casson,†,‡ Tarrah A. Fairweather,† and Irena F.
Creed*,†
†Department of Biology, Western University, 1151 Richmond Street,
London, Ontario Canada, N6A 5B7 ‡University of Winnipeg, Department
of Geography, 515 Portage Avenue, Winnipeg, Manitoba, Canada, R3B
2E9
*S Supporting Information
ABSTRACT: Most forest nitrogen budgets are imbalanced, with
nitrogen inputs exceeding nitrogen outputs. The denitrification
products nitrous oxide (N2O) and dinitrogen (N2) represent
often-unmeasured fluxes that may close the gap between explained
nitrogen inputs and outputs. Gaseous N2O and N2 effluxes, dissolved
N2O flux, and traditionally measured dissolved nitrogen species
(i.e., nitrate, ammonium, and dissolved organic nitrogen) were
estimated to account for the annual nitrogen output along hillslope
gradients from two catchments in a temperate forest. Adding N2O and
N2 effluxes to catchment nitrogen output not only reduced the
discrepancy between nitrogen inputs and outputs (9.9 kg ha−1 yr−1
and 6.5 or 6.3 kg ha−1 yr−1, respectively), but also between
nitrogen outputs from two catchments with different topographies
(6.5 kg ha−1 yr−1 for the catchment with a large wetland, 6.3 kg
ha−1 yr−1 for the catchment with a very small wetland). Dissolved
N2O comprised a very small portion of the annual nitrogen outputs.
Nitrogen inputs exceeded nitrogen outputs throughout the year
except during spring runoff, and also during autumn storms in the
catchment with the large wetland. Failing to account for
denitrification products, especially during summer rainfall events,
may lead to underestimation of annual nitrogen losses.
INTRODUCTION
The global nitrogen (N) cycle has undergone great alterations
during the past century that have resulted in an increase in global
reactive N.1−3 Atmospherically deposited reactive N is currently
estimated at 280 Tg of N yr−1,.4 Several potential fates await this
atmospherically deposited N in forest ecosystems (Figure 1): (1) it
may be assimilated by organisms (micro- organisms and higher); (2)
it may undergo transformations that
include nitrification and denitrification, with nitrous oxide (N2O)
as an obligate intermediate and dinitrogen (N2) as the final
product;5,6 or (3) it may be lost to aquatic systems in hydrologic
flows. The potential fate of atmospherically deposited N is
important because of its potential to become an ecosystem
disservice or service.7 For example, on the one hand,
denitrification of reactive N to N2O is linked to global warming8
and ozone depletion9 (an ecosystem disservice), but on the other
hand, it is linked to removal of dissolved nitrate (NO3
−) from water exiting catchments, thereby shielding receiving
aquatic ecosystems from the effects of NO3
− loading10
(an ecosystem service). A predictive understanding of catchment N
transformations
at different spatial and temporal scales remains a major scientific
challenge.2,11−13 Partitioning N within ecosystems into its
different species based on inputs and outputs is an essential first
step toward quantifying the different forms of N in the system.14
However, our ability to account for the fate of N in catchments is
incomplete.2,13 There remains a portion of atmospherically
deposited N that cannot be accounted for that is often referred to
as the “missing N” in catchment N budgets.2,15
Received: July 25, 2016 Revised: April 13, 2017 Accepted: May 3,
2017 Published: May 3, 2017
Figure 1. Conceptual model showing the different fates of
atmospherically deposited nitrogen: (1) assimilated by organisms
(microorganisms and higher); (2) nitrification and denitrification,
with N2O as an obligate intermediate and N2 as the final product;
or (3) lost to aquatic systems via hydrologic flows.
Article
pubs.acs.org/est
−
and ammonium (NH4 +) output, but more dissolved organic
nitrogen (DON) output than catchments with little or no wetlands.17
However, gaseous N output to the atmosphere provides another
important pathway through which N can leave the catchment.11,18
There have been relatively few catchment- scale determinations of N
gas outputs in forests as N gas effluxes are not routinely
integrated into forest N budgets. Recent studies have observed that
rain induced bursts of N2O and N2 efflux during the snow-free
period19 and N2O efflux beneath a snowpack20 are significant
sources of N gas in forests. Not considering this pathway may
contribute to the failure to close N input-output budgets in
catchments.15
The central premise of this paper is that improved estimates of
soil N2O and N2 efflux from forested landscapes require
consideration of topographic controls on N cycling and routing
processes. Topography influences N transformations by controlling
soil temperature, moisture, and redox conditions, and regulates
dissolved organic carbon and NO3
− availability while helping create redox conditions required for N
transformations including denitrification and nitrification to
occur. We test the following hypotheses: (1) the major difference
in N output among catchments is due to variations in the flux of
gaseous N (N2O + N2); and (2) factoring gaseous and dissolved N
outputs narrows the gap in catchment input- output N budgets. We
test these hypotheses in catchments located in a temperate forest,
and expect that the findings will help assess the ability of
temperate forests to process the reactive loads of N, understand
the relative importance of dissolved vs gaseous effluxes from
catchments N budgets, and close the N input vs output N budget of
catchments.
MATERIALS AND METHODS
Study Area. The Turkey Lakes Watershed is a 10.5 km2
watershed located near the eastern shore of Lake Superior in the
Algoma Highlands of Central Ontario (47°03′00″N, 84°25′00″W), 60 km
north of Sault Ste. Marie in the Great Lakes-St. Lawrence forest
region (Figure 2). The watershed receives an average annual
precipitation of
1189 mm with an average annual temperature of 4.6 °C (1981−2010).
The bedrock of the watershed is greenstone with small outcrops of
granite.21 A thin discontinuous till of varying depth overlays the
bedrock with depths ranging from <1 m at high elevations, 1−2 m
at lower elevations, and occasionally up to 65 m in depressions.
Dispersed pockets of Ferric Humisols are found in
bedrock-controlled depressions and adjacent to streams and lakes,
and Orthic Ferro-Humic and Humo-Ferric podzolic soils are
dominant.22 The watershed contains uneven- aged, mature- to
overmature, old-growth forest. The temperate forest is dominated
(90%) by sugar maple (Acer saccharum Marsh.), with yellow birch
(Betula alleghaniensis Britton), white pine (Pinus strobus L.),
white spruce (Picea glauca Moench Voss), ironwood (Ostrya
virginiana (Mill.) K. Koch), and red oak (Quercus rubra L.) in the
upland areas. Sugar maple also dominates in the wetland areas where
it is mixed with eastern white cedar (Thuja occidentalis L.), black
ash (Fraxinus nigra Marsh.), and balsam fir (Abies balsamea (L.)
Mill.).23
Watershed monitoring was established in 1980 to study the effects
of atmospheric deposition on both terrestrial and aquatic
ecosystems.24,25 While there has been a significant decline in
sulfur deposition since the 1980s, N deposition has remained
relatively stable up to and including the period of this
study.26
Catchment 38 (C38) and catchment 35 (C35) are two north- facing
catchments in the Turkey Lakes Watershed in close proximity (∼1 km
apart) that receive similar N inputs. Topography is the main
difference between the two catch- ments: a large wetland (1.58 ha)
covers 25% of the 6.33 ha area of the more gently sloped C38 (13.5°
average slope), while a very small wetland (0.03 ha) covers <1%
of the 3.12 ha area of
Figure 2. Map of the Turkey Lakes Watershed in Central Ontario,
Canada with the two catchments used in the present study (C38 and
C35). (Maps created in Creed laboratory).
Environmental Science & Technology Article
the relatively steeper C35 (19.1° average slope) (Figure 2). This
work builds on previous studies that reported differences in
dissolved N output among catchments in the forested landscape of
the Great Lakes-St. Lawrence forest region at the northern edge of
the temperate forest biome of North America.16,27−29
Experimental Design. Total (wet and dry) N inputs were collected at
the Canadian Air and Precipitation Monitoring Network (CAPMoN) site
located closest to the catchments. Total (gaseous and dissolved) N
outputs were sampled in C35 and C38 from 2005 to 2010 water years
(June 1 to May 30). In c38, soil N2O efflux measurements were
collected along hillslope gradients of inner wetland (IW), outer
wetland (OW), lowland (LOW), and upland (UP) positions derived from
a LiDAR-based 5 m digital elevation model using digital terrain
analysis methods.30 Soil N2O efflux measurements were collected
between 64 and 72 times per position during the snow-free season
(June to September) from 2006 to 2010 using ground-based static
chambers.19 Soil N2O efflux measurements were collected between 36
and 40 times per position during the snow season (October to May)
in 2006/2007 from sampling ports attached at different depths along
1.25 m PVC tubes inserted into the snowpack.20 Daily soil N2 efflux
was estimated using the acetylene-inhibition technique in the IW
and OW positions for 1 day during the snow-free season of 2010.
Dissolved NH4
+, NO3 −, and DON concentrations were
measured from water samples collected at weirs at the outlets of
both C38 and C35 in the 2005 to 2010 water years, and dissolved N2O
concentrations were measured from water samples collected at weirs
at the outlets of both catchments in the 2006 water year. The
median and 25th and 75th percentiles of estimates of N2O and N2 in
the snow and snow-free seasons in C38 are given in Table 1.
Dissolved NH4
+, NO3 −, DON, and
N2O fluxes were calculated by multiplying concentrations by stream
discharge. Sampling and analytical methods have been described
fully in other publications19,20,31 and are summarized in the
Supporting Information (SI). Data Analyses. Daily outputs estimated
from flux measure-
ments taken at irregular intervals were summed to generate monthly
and annual N outputs for the 2005 to 2010 water years. Daily soil
N2O effluxes were measured in the IW, OW, LOW, and UP positions in
C38 at daily to monthly intervals during the snow-free (June to
September) season and at daily to bimonthly intervals during snow
season (October to May) in the 2005 to 2010 water years. Dissolved
stream NO3
−, NH4 +,
and DON fluxes were measured in C35 and C38 at daily to biweekly
intervals in the 2005 to 2010 water years. Several methods were
applied to derive daily soil and
dissolved N flux estimates on all days for the 2005 to 2010 water
years from measured values. Regressions using daily precipitation
as the independent
variable were used to model daily soil N2O effluxes for rain days
during the snow-free season (i.e., when (1) effective precipitation
(same day plus previous day, in order to capture rainfall that may
have fallen during the night) exceeded 3 mm,32
and (2) when the water table depth was less than 10 mm) at the IW
and OW positions. Separate models were developed for each of the IW
and OW positions based on 14 rain day observations of N2O efflux
from each position.19,33
No significant relationships were observed between environ- mental
drivers (temperature or precipitation) and soil N2O effluxes at the
IW or OW positions on nonrain days or at the LOW or UP positions.
Soil N2O effluxes at the IW and OW positions on nonrain days in the
snow-free season were infilled on days with no measurements using
median values from the distributions of measured snow-free season
N2O effluxes on nonrain days at each position. Soil N2O effluxes at
the LOW and UP positions on both rain and nonrain days in the snow-
free season were infilled on days with no measurements using median
values from the distributions of measured snow-free season N2O
effluxes on both rain and nonrain days at each position. Soil N2O
effluxes at all positions in the snow season were infilled on days
with no measurements by using median values from the distributions
of measured snow season N2O effluxes at each position. Daily N2
effluxes at the IW and OW positions on rain days in
the snow-free season were calculated using measured snow-free
season rain day N2:N2O ratios at each position which were then
multiplied by the daily estimated N2O efflux (if estimated N2O
efflux was negative, N2 efflux was given as zero). N2 efflux was
not estimated during nonrain days in the IW and OW or in the UP and
LOW as minimal denitrification was assumed under the dry conditions
that these days and positions represent.19
Daily dissolved N2O fluxes were estimated using median values
derived from the distribution of measured dissolved N2O
concentrations multiplied by daily discharge. Missing dissolved
NH4
+, NO3 −, and DON were infilled using linear interpolation.
Daily soil N2O and N2 efflux estimates were multiplied by the
respective areas of the IW, OW, LOW, and UP positions in each
catchment (Figure 2) and summed to estimate daily catchment N2O and
N2 output estimates. Monthly and annual
Table 1. Medians and the 25th and 75th Percentiles of Distributions
of Soil N2O and N2 (mg ha−1 d−1) Effluxes Across a Hillslope
Gradient and Stream N2O Fluxes at the Catchment Outlet in C38
snow-free season (no rain) snow-free season (rain >3 mm and
WTD
<10mm) snow season
soil N2O 25th percentile median 75th percentile 25th percentile
median 75th percentile 25th percentile median 75th percentile IW
4044 5496 8391 4368 7703 18 009 683 1139 2252 OW 5552 8145 14 507
10 816 25 915 54 809 706 1293 2736 LOW 2880 5487 9773 2442 4216
5458 986 1214 2310 UP 2350 5133 7248 1129 2841 3911 733 1315
2160
soil N2
IW 85 611 150 986 352 981 13 382 22 315 44 109 OW 109 237 261 738
553 575 7104 13 007 27 528
stream N2O 0.00003 0.00018 0.00425 0.00001 0.00140 0.00266 2.96
7.56 34.95
Environmental Science & Technology Article
− + NH4 +) and
DON for each year. Differences in measured daily N2O and total
gaseous N (N2O + N2) effluxes at different positions were assessed
using ANOVAs on ranks with Post-Hoc Dunn’s tests. Data analyses
were performed using SigmaPlot 12 (Systat Software, San Jose,
CA).
RESULTS Atmospheric N inputs were much greater than N outputs,
particularly when only DIN and DON output sources were considered
(Figure 3). Dissolved N outputs were smaller in
C38 than in C35, primarily due to less DIN output from C38 (Figure
3). Dissolved N2O export in the stream was extremely small during
both the snow-free and snow seasons and therefore not considered
further (Figure 4), and the differences in dissolved N outputs were
maintained when gaseous N2O + N2 efflux was included for the IW and
OW positions (Figure 4, bottom). Average monthly sums of daily
efflux estimates revealed
peaks in DIN and DON outputs in spring and, to a lesser extent,
autumn (Figure 5). These peaks coincided with periods of high
catchment discharge during spring snowmelt and autumn storms. In
contrast, peaks in N2O and N2 outputs were revealed in the summer
(Figure 5). Catchment 38 generated more dissolved organic N and
gaseous N2O + N2 output, whereas C35 generated more inorganic N
output, dominated by NO3
−. Total soil N2O efflux during the snow-free season was
similar
for the two catchments (0.8 kg N ha−1 yr−1 in C38 vs 0.6 kg N ha−1
yr−1 in C35), whereas N2 efflux estimates were much greater in C38
(1.5 kg N ha−1 yr−1) than in C35 (0.06 kg N ha−1 yr−1). Similarly,
total soil N2O efflux during the snow season was similar for the
two catchments (0.3 kg N ha−1 yr−1
in C38 and C35), whereas total soil N2 efflux was greater in C38
(1.0 kg N ha−1 yr−1) than in C35 (0.04 kg N ha−1 yr−1). There was
considerably more output of DON and DIN in the snow season compared
to the snow-free season. Furthermore,
there was considerably more output of DON, less output of NO3
−, but similar output of NH4 + in C38 compared to C35.
The average annual N output from the two catchments was similar
when gaseous N2 and N2O were added to the dissolved N output
(Figure 3). The average annual N input was 9.9 kg N ha−1 yr−1, and
the average annual N output was 6.5 kg N ha−1
yr−1 from C38 (66% of N input) vs 6.3 kg ha−1 yr−1 from C35 (64% of
N input). The composition of the average annual N output differed,
with N2O + N2 comprising 55% of N output from C38, but only 16%
from C35. The NO3
−, NH4 +, and
DON comprised the remaining 45% of N output from C38 and 84% of N
output from C35.
DISCUSSION Estimates of catchment N inputs vs N outputs are
important because they provide insights on the functioning of a
forest ecosystem. This is particularly important when considering
the ecosystem effects of atmospheric N deposition that has been
elevated since the industrial revolution12,34 and the potential
fate of this elevated atmospheric N deposition on forests35 and
associated downstream waters.7,36,37 Yet most studies have reported
catchment N inputs that have often far exceeded N outputs, leaving
in question the fate of the “missing” N in these catchment N
budgets. This paper examined the role of gaseous N2O and N2
effluxes
in N budget estimates in a temperate forest. Nitrogen output was
compared in two catchments, one with 25% wetland (C38) and one with
<1% wetland (C35). When considering DIN and DON output only, 2.9
kg N ha−1 yr−1 was exported from C38, whereas 5.3 kg N ha−1 yr−1
was exported from C35. This represented only 30% (C38) and 54%
(C35) of the 9.9 kg N ha−1 yr−1 that was atmospherically deposited
onto the catchment. However, when gaseous N2O and N2 effluxes were
incorporated in the N budgets, the N outputs were similar; this
represents a reduction of 90% of the difference between the two
catchments. Although the difference in N output between the
catchments was diminished, the proportion of different N species
that comprised these N budgets was different due to the different
area proportions of wetlands, suggesting differences in the
predominance of N transformation processes within the
catchments.
The Missing Nitrogen of Nitrogen Budgets. Incorpo- rating gaseous
and dissolved N species had two effects on the N budgets: (1) it
closed the gap in N output between C38 and C35 as indicated above;
and (2) it narrowed the gap between N input and N output in both
catchments. Gaseous N2O efflux contributed 17% in C38 and 14% in
C35
to the total N output, and gaseous N2 efflux contributed an
additional 38% in C38 and 2% in C35 to the total N output. The
combined gaseous N2O + N2 output represented 36% in C38 and 10% in
C35 of the total atmospherically deposited N, within reasonable
range of Bouwman et al.4 who estimated N2O + N2 output as 40% of
atmospherically deposited N. Wetlands are a considerable source of
N2O and N2, highlighting the importance of wetlands in mitigating
the accumulation of atmospherically deposited N during late summer,
but not during winter. Dissolved N2O efflux was less than 1% of the
total N2O efflux in both catchments, consistent with observations
made by Davidson and Swank,38 suggesting that dissolved N2O efflux
to streams may not be a substantial pathway of N output in forested
catchments. There was less NO3
− output from C38 (15% of total N output) than C35 (76% of total N
output), which suggests that
Figure 3. Average annual N budget for 2005 to 2010 in the C38 and
C35 catchments in the Turkey Lakes Watershed showing traditionally
measured N species, including dissolved inorganic nitrogen (DIN,
nitrate-N + ammonium-N) and dissolved organic nitrogen (DON), as
well as gaseous and dissolved nitrous oxide (N2O) and dinitrogen
(N2) efflux. Error bars represent the standard deviations of N
outputs with the gray shaded area representing the standard
deviation of N inputs.
Environmental Science & Technology Article
NO3 − is not being hydrologically flushed from C38,28 but
rather is stored in the wetland and then transformed to other forms
of N.17 The NO3
+
output from both catchments (0.06 kg ha−1 yr−1 or 1% of total N
output in C38 and 0.07 kg ha−1 yr−1 or 1% of total N output in
C35). There was more DON output in C38 (29% of the total N output)
than C35 (8% of the total N output). These observations are
consistent with those made in other catchments of the Turkey Lakes
Watershed.14 While most of the dissolved N output coincided with
spring melt, interception of the drainage waters by the wetland in
C38 likely resulted in the retention and conversion of N to other
forms (e.g., DON).41 Dissolved inorganic and organic N that
accumulates during the winter can then be converted to gaseous N2O
and N2 during warmer conditions in the summer.41,42
Topography influences the atmospheric vs aquatic fate of N. The
catchment with the large wetland (C38) had much greater gaseous N2O
and N2 output than the catchment with a small wetland. During the
snow season, N2O and N2 efflux occurred continuously, while during
the snow free season, bursts of N2O efflux occurred in response to
rain events.19 However, these differences between the catchments
were mitigated by considerable N2O efflux beneath the snowpack,
where there was no observed difference in N2O efflux among the
different positions.20 Therefore, both C38 and C35 produced
substantial amounts of N2O during the snow season (0.5 kg ha−1
yr−1).
Total annual gaseous N2O efflux estimates from the two catchments
for the years 2005 to 2010 ranged from 0.8 to 1.7 kg N ha−1 yr−1 in
C38 and from 0.5 to 1.6 kg N ha−1 yr−1 in C35; these estimates are
reasonably similar to the values reported for a temperate forest in
the United States (0.3−1.4 kg N ha−1 yr−1)15 and a temperate forest
in Germany (0.2−7.1 kg N ha1 yr−1).43 Previous studies showed that
topographic indicators of hydrologic storage potential (i.e.,
effects of topographic flats and depressions on water storage) were
the best predictors of DON output in catchments of the Turkey Lakes
Watershed, and topographic indicators of both hydro- logic storage
potential and hydrologic flushing potential (i.e., the effects of
topographic slopes on the potential for variable source areas to
expand and tap into previously untapped areas) were the best
predictors of NO3
− output.16,17 Hydrologic flushing potential may not be a good
predictor of dissolved N2O and N2 output, because large
precipitation events promote the formation of N2O and N2 and rapid
off-gassing of N before it can reach the catchment outlet.19
However, hydrologic storage potential might also be a good
predictor of gaseous N2O and N2 output.
Remaining Missing Nitrogen in Nitrogen Budgets. Incorporating
gaseous N2O and N2 narrowed the gap between N inputs and outputs,
but the average annual N input was still approximately 3.5 kg N
ha−1 yr−1 greater than average annual N output. Neither the shallow
soil, the partially decomposed leaf matter
litter nor the tree biomass is likely to be a significant
long-term
Figure 4. Daily measured N2O (top) and N2 (bottom) efflux estimates
across a hillslope gradient in C38 during the snow-free season
(June to September) from 2005 to 2010 (left) and during the snow
season in October 2006 to May 2007 (right). N2 was not measured in
stream and at the LOW and UP positions. Different letters indicate
significant differences among topographic positions (p <
0.05).
Environmental Science & Technology Article
sink for N in this temperate forest ecosystem. For shallow soil,
repeated sampling of the upper soil horizons over the past 25 years
has shown that, while there is significant variability both
year-to-year and across the landscape, total N content in these
pools has not increased significantly.44−46 For litter, Morrison
and Foster47 observed an increase in litter N pools over a 15- year
period, but attributed it to immobilization from upper soil layers
and therefore not an absolute increase in the litter-soil pool. The
low carbon:nitrogen (C:N) and high nitrification rates in soils
associated with sugar maple forests mean that most of the N is
converted to NO3
− which is a mobile form of N that is either exported to the stream
or converted to gaseous forms through denitrification,14 reducing
likelihood of N retention in these soils. Tree biomass may also be
a significant long-term sink for N. However, while N pools in tree
biomass have not been reported at the Turkey Lakes Watershed since
the 1980s, reports from mature temperate forests in eastern North
America suggest that N pools in forest biomass are not likely to be
significant sinks at this late stage of forest
development.15,48
There are several uncertainties in our N budget calculations.
First, dry deposited N that falls on leaf surfaces may not reach
the forest floor, but may be processed on the leaf surface.49
Second, gaseous N might evade to the atmosphere via a pathway not
measured, including transpiration of dissolved N2O in soil water,50
volatilization of NH4
+, or off-gassing of dissolved N2O from the stream.51 Third, N
might be sequestered in deeper soil horizons not captured in the
soil surveys.52 Soils in the Turkey Lakes Watershed are typically
shallow, but pockets of deeper soils exist, particularly in the
wetlands, where anaerobic conditions promote accumulation of
organic N and NH4
+, which may act as a long-term sink for N.
There are also factors that could increase the discrepancy between
inputs and outputs in our calculations. We did not account for N
fixation as a possible input. Published rates of N fixation in
temperate forests suggest that this is a minor input,53
but measurements are sparse and uncertain.52 Furthermore, we did
not estimate N2 efflux from upland positions or from wetland
positions on nonrain days during the growing season. While N2O
efflux numbers for these positions during these time periods
suggest that denitrification rates are likely low, this could mean
that our estimate of N2 efflux is conservative. Finally, we did not
account for significant N storage in the soil. However, if N
storage did occur, it likely occurred at a similar rate within each
of the two catchments, and therefore the effect of N storage on the
N budget would have been similar in the two catchments. While there
remains some missing portion of atmospherically
deposited N, accounting for N2O and N2 narrowed the observed
differences in N outputs between catchments with and without
wetlands. The presence of wetlands contributes gaseous N products
(N2O and N2) to the composition of N outputs from catchments due to
the presence of reducing conditions (lower redox potentials). These
gaseous N products account for substantial amounts of both
atmospherically deposited N (10−36% of N input) and N in discharge
waters (16−55% of N output). While these results demonstrate the
importance of gaseous N products to N budgets in temperate forests,
scaling this process up across the region remains a significant
challenge.12 A process-based understanding that considers
topographic influences on N transformations is key to estimating
these elusive fluxes. Future work on resolving N budgets in
forested catchments can use the topographic framework presented
here to help constrain this highly heterogeneous process.
ASSOCIATED CONTENT *S Supporting Information The Supporting
Information is available free of charge on the ACS Publications
website at DOI: 10.1021/acs.est.6b03728.
Detailed methods for atmospheric N input and gaseous and dissolved
N output measurements (PDF)
AUTHOR INFORMATION Corresponding Author *Phone: 1-519-661-4265;
fax: 1-519-661-3935; e-mails:
[email protected]. ORCID Irena F. Creed:
0000-0001-8199-1472 Notes The authors declare no competing
financial interest.
ACKNOWLEDGMENTS This research was funded by an NSERC Discovery
grant to Irena Creed (217053-2009 RGPIN). Data are available by
contacting Irena Creed (
[email protected]). The Canadian Forest
Service, Natural Resources Canada, provided discharge and chemistry
data (Fred Beall), and Environment Canada and Climate Change,
provided meteorological data (Dean Jeffries) and atmospheric
nitrogen deposition data (Robert Vet).
REFERENCES (1) Vitousek, P. M.; Aber, J. D.; Howarth, R. W.;
Likens, G. E.; Matson, P. A.; Schindler, D. W.; Schlesinger, W. H.;
Tilman, D. G.
Figure 5. Monthly total N outputs for the C38 and C35 catchments
from 2005 to 2010 in the Turkey Lakes Watershed.
Environmental Science & Technology Article
Technical report: Human alteration of the global nitrogen cycle:
Sources and consequences. Ecol. Appl. 1997, 7, 737−750. (2)
Galloway, J. N.; Dentener, F. J.; Capone, D. G.; Boyer, E. W.;
Howarth, R. W.; Seitzinger, S. P.; Asner, G. P.; Cleveland, C. C.;
Green, P. A.; Holland, E. A.; et al. Nitrogen cycles: past,
present, and future. Biogeochemistry 2004, 70, 153−226. (3)
Rockstrom, J.; Steffen, W.; Noone, K.; Persson, Å.; Chapin, F. S.,
III; Lambin, E. F.; Lenton, T. M.; Scheffer, M.; Folke, C.;
Schellnhuber, H. J.; et al. A safe operating space for humanity.
Nature 2009, 461, 472−475. (4) Bouwman, A. F.; Beusen, A. H. W.;
Griffioen, J.; Van Groenigen, J. W.; Hefting, M. M.; Oenema, O.;
Van Puijenbroek, P. J. T. M.; Seitzinger, S.; Slomp, C. P.;
Stehfest, E. Global trends and uncertainties in terrestrial
denitrification and N2O emissions. Philos. Trans. R. Soc., B 2013,
368, 20130122. (5) Gambrell, R. P.; Patrick, Jr., W. H. Chemical
and microbiological properties of anaerobic soils and sediments, In
Plant Life in Anaerobic Environments; Hook, D. D., Crawford, R. M.,
Eds.; Ann Arbor Sci. Pub. Inc.: Ann Arbor, MI, 1978. (6) Fowler,
D.; Pilegaard, K.; Sutton, M. A.; Ambus, P.; Raivonen, M.; Duyzer,
J.; Simpson, D.; Fagerli, H.; Fuzzi, S.; Schjoerring, J. K.; et al.
Atmospheric composition change: Ecosystems-atmosphere interactions.
Atmos. Environ. 2009, 43, 5193−5267. (7) Burgin, A. M.; Lazaar, J.
G.; Groffman, P. M.; Gold, A. J.; Kellog, D. Q. Balancing nitrogen
retention ecosystem services and greenhouse gas disservice at the
landscape scale. Ecol. Eng. 2013, 56, 26−35. (8) IPCC. Climate
Change 2013: The Physical Science Basis. Contribution of Working
Group I to the Fifth Assessment Report of the Intergovernmental
Panel on Climate Change; Stocker, T. F. et al., Eds.; Cambridge
University Press: New York, 2013. (9) Ravishankara, A. R.; Daniel,
J. S.; Portmann, R. W. Nitrous Oxide (N2O): The dominant
Ozone-depleting substance emitted in the 21st century. Science
2009, 326, 126. (10) Mosier, A. R.; Kroeze, C.; Nevison, C.;
Oenema, O.; Seitzinger, S.; van Cleemput, O. Closing the global N2O
budget: nitrous oxide emissions through the agricultural nitrogen
cycle. Nutr. Cycling Agroecosyst. 1998, 52, 225−248. (11) Groffman,
P. M.; Butterbach-Bahl, K.; Fulweiler, R. W.; Gold, A. J.; Morse,
J. L.; Stander, E. K.; Tague, C.; Tonitto, C.; Vidon, P. Challenges
to incorporating spatially and temporally explicit phenomena
(hotspots and hot moments) in denitrification models.
Biogeochemistry 2009, 93, 49−77. (12) Davidson, E. A.; David, M.
B.; Galloway, J. N.; Goodale, C. L.; Haeuber, R.; Harrison, J. A.;
Howarth, R. W.; Jaynes, D. B.; Lowrance, R. R.; Nolan, B. T.; et
al. Excess nitrogen in the U.S. environment: Trends, risks, and
solutions. ESA Issues Ecol. 2012, 15, 1−16. (13) Duncan, J. M.;
Groffman, P. M.; Band, L. E. Towards closing the watershed nitrogen
budget: Spatial and temporal scaling of denitrification. J.
Geophys. Res.: Biogeosci. 2013, 118, 1105−1119. (14) Foster, N.;
Spoelstra, J.; Hazlett, P.; Schiff, S.; Beall, F. D.; Creed, I. F.;
David, C. Heterogeneity in soil nitrogen within first-order
forested catchments at the Turkey Lakes Watershed. Can. J. For.
Res. 2005, 35, 797. (15) Yanai, R. D.; Vadeboncoeur, M. A.;
Hamburg, S. P.; Arthur, M. A.; Fuss, C. B.; Groffman, P. M.;
Siccama, T. G.; Driscoll, C. T. From missing source to missing
sink: Long-term changes in the nitrogen budget of a northern
hardwood forest. Environ. Sci. Technol. 2013, 47, 11440−11448. (16)
Creed, I. F.; Beall, F. D. Distributed topographic indicators for
predicting nitrogen export from headwater catchments. Water Resour.
Res. 2009, 45, 1−12. (17) Mengistu, S. G.; Creed, I. F.; Webster,
K. L.; Enanga, E.; Beall, F. D. Searching for similarity in
topographic controls on carbon, nitrogen and phosphorus export from
forested headwater catchments. Hydrol. Process. 2014, 28,
3201−3216. (18) Goodale, C. L.; Fredriksen, G.; Weiss, M. S.;
McCalley, C. K.; Sparks, J. P.; Thomas, S. A. Soil processes drive
seasonal variation in retention of 15N tracers in a deciduous
forested catchment. Ecology 2015, 96, 2653−2668.
(19) Enanga, E. M.; Creed, I. F.; Casson, N. J.; Beall, F. D.
Summer storms trigger soil N2O efflux episodes in forested
catchments. J. Geophys. Res.: Biogeosci. 2016, 121, 95−108. (20)
Enanga, E. M.; Creed, I. F.; Fairweather, T.; Casson, N. J.; Beall,
F. D. Snow covered soils produce N2O that is lost from forested
catchments. J. Geophys. Res.: Biogeosci. 2016, 121, 2356−2368. (21)
Jeffries, D. S.; Kelso, J. R. M.; Morrison, I. K. Physical,
chemical, and biological characteristics of the Turkey Lakes
Watershed, central Ontario, Canada. Can. J. Fish. Aquat. Sci. 1988,
45, 3−13. (22) Canada Soil Survey Committee. Canadian System of
Soil Classification; Department of Agriculture: Ottawa, Ontario,
Canada, 1978. (23) Wickware, G. M.; Cowell, D. W. Forest ecosystem
classification of the Turkey Lakes Watershed, Ontario. Environ.
Cons. Serv., Lands Dir., Eco. Land. Class. Ser. 1985, 18, 33. (24)
Kelso, J. R. M. Preface. Can. J. Fish. Aquat. Sci. 1988, 45, 2.
(25) Jeffries, D. S. Foreword, The Turkey Lakes Watershed Study
after two decades. Water, Air, Soil Pollut.: Focus 2002, 2, 1−3.
(26) Mengistu, S. G.; Quick, C. G.; Creed, I. F. Nutrient export
from catchments on forested landscapes reveals complex
nonstationary and stationary climate signals. Water Resour. Res.
2013, 49, 1−18. (27) Creed, I. F.; Band, L. E.; Foster, N. W.;
Morrison, I. K.; Nicolson, J. A.; Semkin, R. S.; Jeffries, D. S.
Regulation of nitrate-N release from temperate forests: A test of
the N flushing hypothesis. Water Resour. Res. 1996, 32, 3337−3354.
(28) Creed, I. F.; Band, L. E. Exploring functional similarity in
the export of nitrate-N from forested catchments: A mechanistic
modeling approach. Water Resour. Res. 1998, 34, 3079−3093. (29)
Creed, I. F.; Band, L. E. Export of nitrogen from catchments within
a temperate forest: evidence for a unifying mechanism regulated by
variable source area dynamics. Water Resour. Res. 1998, 34, 3105−
3120. (30) Webster, K. L.; Creed, I. F.; Beall, F. D.;
Bourbonniere, R. A. A topographic template for estimating soil
carbon pools in forested catchments. Geoderma 2011, 160, 457−467.
(31) Sirois, A.; Vet, R. Detailed analysis of sulphate and nitrate
atmospheric deposition estimates at the Turkey Lakes Watershed.
Can. J. Fish. Aquat. Sci. 1988, 45, 14−25. (32) Kulkarni, M. V.;
Groffman, P. M.; Yavitt, J. B.; Goodale, C. L. Complex controls of
denitrification at ecosystem, landscape and regional scales in
northern hardwood forests. Ecol. Modell. 2015, 298, 39−52. (33)
Snedecor, G. W., Cochran, W. G. Statistical Methods, 8th ed.; Iowa
State University Press: Ames, IA, 1989. (34) Galloway, J. N.;
Townsend, A. R.; Erisman, J. W.; Bekunda, M.; Cai, Z.; Freney, J.
R.; Martinelli, L. A.; Seitzinger, S. P.; Sutton, M. A.
Transformation of the nitrogen cycle: recent trends, questions, and
potential solutions. Science 2008, 320, 889−892. (35) Yanai, R. D.;
Tokuchi, N.; Campbell, J. L.; Green, M. B.; Matsuzaki, E.; Laseter,
S. N.; Brown, C. L.; Bailey, A. S.; Lyons, P.; Levine, C. R.; Buso,
D. C.; Likens, G. E.; Knoepp, J.; Fukushima, K. Sources of
uncertainty in estimating stream solute export from headwater
catchments at three sites. Hydrol. Process. 2015, 29, 1793− 1805.
(36) Kliewer, B. A.; Gilliam, J. W. Water table management effects
on denitrification and nitrous oxide evolution. Soil Sci. Soc. Am.
J. 1995, 59, 1694−1701. (37) Vidon, P.; Hubbard, L. E.; Soyeux, E.
Seasonal solute dynamics across land uses during storms in
glaciated landscape of the US Midwest. J. Hydrol. 2009, 376, 34−47.
(38) Davidson, E. A.; Swank, W. T. Nitrous oxide dissolved in soil
solution: An insignificant pathway of nitrogen loss from a
southeastern hardwood forest. Water Resour. Res. 1990, 26,
1687−1690. (39) Davidson, E. A.; Chorover, J.; Dail, D. B. A
mechanism of abiotic immobilization of nitrate in forest
ecosystems: the ferrous wheel hypothesis. Glob. Change Biol. 2003,
9, 228−236. (40) Wrage, N.; Velthof, G. L.; van Beusichem, M. L.;
Oenema, O. Role of nitrifier denitrification in the production of
nitrous oxide. Soil Biol. Biochem. 2001, 33, 1723−1732.
Environmental Science & Technology Article
(41) Farquharson, R.; Baldock, J. Concepts in modelling N2O
emissions from land use. Plant Soil 2008, 309, 147−167. (42)
Holtan-Hartwig, L.; Dorsch, P.; Bakken, L. R. Low temperature
control of soil denitrifying communities: kinetics of N2O
production and reduction. Soil Biol. Biochem. 2002, 34, 1797−1806.
(43) Brumme, R.; Borken, W.; Finke, S. Hierarchical control on
nitrous oxide emission in forest ecosystems. Glob. Biogeochem.
Cycles 1999, 13, 1137−1148. (44) Morrison, I. K. Organic matter and
mineral distribution in an old-growth Acer saccharum forest near
the northern limit of its range. Can. J. For. Res. 1990, 20,
1332−1342. (45) Creed, I. F.; Trick, C. G.; Band, L.; Morrison, I.
K. Characterizing the spatial pattern of soil carbon and nitrogen
pools in the Turkey Lakes Watershed: a comparison of regression
techniques. Water, Air, Soil Pollut.: Focus 2002, 2, 81−102. (46)
Webster, K. L.; Creed, I. F.; Bourbonniere, R. A.; Beall, F. D.
Controls on the heterogeneity of soil respiration in a tolerant
hardwood forest. J. Geophys. Res. 2008, 113, 1−15. (47) Morrison,
I. K.; Foster, N. W. Fifteen-year change in forest floor organic
and element content and cycling at the Turkey Lakes Watershed.
Ecosystems 2001, 4, 545−554. (48) Watmough, S. A.; Dillon, P. J.
Major element fluxes from a coniferous catchment in central
Ontario, 1983−1999. Biogeochemistry 2004, 67, 369−399. (49) Uscola,
M.; Villa-Salvador, P.; Oliet, J.; Warren, C. R. Foliar absorption
and root translocation of nitrogen from different chemical forms in
seedlings of two Mediterranean trees. Environ. Exp. Bot. 2014, 104,
34−43. (50) Mosier, A. R.; Mohanty, S. K.; Bhadrachalam, A.;
Chakravorti, S. P. Evolution of dinitrogen and nitrous oxide from
the soil to the atmosphere through rice plants. Biol. Fertil. Soils
1990, 9, 61−67. (51) Baulch, H. M.; Schiff, S. L.; Maranger, R.;
Dillon, P. J. Nitrogen enrichment and the emission of nitrous oxide
from streams. Glob. Biogeochem. Cycles 2011, 25, GB4013. (52)
Johnson, D. W.; Turner, J. Nitrogen budgets of forest ecosystems: A
review. For. Ecol. Manage. 2014, 318, 370−379. (53) Roskoski.
Nitrogen fixation in hardwood forests of the northeastern United
States. Plant Soil 1980, 54, 33−44.
Environmental Science & Technology Article