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Soil Biology & Biochemistry 32 (2000) 1431±1441
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Sensitivity of soil methane ¯uxes to reduced precipitation in
boreal forest soils
S.A. Billings a,*, D.D. Richter b, J. Yarie c
a

Biological Sciences Department, University of Arkansas, Fayetteville, AR 72701, USA
b
Nicholas School of the Environment, Duke University, Durham, NC 22708, USA
c
University of Alaska Fairbanks, School of Agriculture and Land Resource Management, Fairbanks, AK 99775, USA
Received 4 August 1999; received in revised form 25 January 2000; accepted 14 February 2000

Abstract
In order to better predict soil sinks of methane, we need to examine soil methane ¯ux patterns and responses to altered soil
moisture regimes. Estimates of the global atmospheric CH4 budget must also account for ¯uxes in the vast boreal region. We
measured methane ¯uxes into the soil surface, methane concentrations, water content, and temperature in the soil pro®le in two
interior Alaskan forests, over two growing seasons. At each site, a 0.10 ha rain-shelter limited summer precipitation from
entering the soil. Limiting summer precipitation at the upland site generally increased that site's soil uptake of methane. Average

rates of soil methane uptake among upland plots ranged from 0.10 to 0.95 mg mÿ2 dayÿ1. At the ¯oodplain site, limiting
precipitation decreased the soil methane uptake of that site, and the rates here ranged from ÿ0.02 to 0.57 mg mÿ2 dayÿ1. Using
soil pro®le methane concentrations, we calculated CH4 ¯uxes using Fick's Law. Our inability to precisely measure the
concentration gradient across the soil surface resulted in calculated ¯ux estimates that more likely represent ¯uxes within the soil
pro®le. Methane sources and sinks in the soil pro®le also confounded the comparison of measured and calculated ¯uxes. 7 2000
Elsevier Science Ltd. All rights reserved.
Keywords: Soil methane consumption; Boreal forest soils; Fick's Law; Soil moisture; Methanotrophy; Methanogenesis

1. Introduction
The atmospheric concentration of methane is currently increasing at a rate of about 1% per year (Torn
and Harte, 1996). Since methane is a greenhouse gas,
studies on the role of soil as a sink for atmospheric
methane have been conducted in temperate forests
(Steudler et al., 1989; Yavitt et al., 1990; King and
Adamsen, 1992; Dorr et al., 1993; Castro et al., 1994;
Hutsch et al., 1994; Schnell and King, 1994; Bender
and Conrad 1995; Ambus and Christensen, 1995;
Sitaula et al., 1995; Castro et al., 1995; Yavitt et al.,
1995), boreal forests (Whalen et al., 1991; Whalen et

* Corresponding author. Tel.: +1-501-575-2227; fax: +1-501-5754010.
E-mail address: sbillin@comp.uark.edu (S.A. Billings).

al., 1992; Castro et al., 1993; Whalen and Reeburgh,
1996; Gulledge et al., 1997; Gulledge and Schimel,
1998a, 1998b), arctic tundra (Whalen and Reeburgh,
1988; Whalen and Reeburgh, 1990a, 1990b; Schimel,
1995), montane soils (Torn and Harte, 1996), tropical
soils (Keller et al., 1983, Keller et al., 1986; Dorr et
al., 1993), and deserts (Striegl et al., 1992). About 10 
1012g yearÿ1 of methane are consumed by soil microbes globally (Schlesinger, 1991).
Some evidence suggests that physical and not biological controls govern the oxidation capacity of soils:
methane ¯uxes into soils often show only a slight temperature response (Born et al., 1990). Increased soil
moisture often decreases soil methane uptake (Mosier
et al., 1991), which could indicate limited microbial
access to CH4. In addition, soil methane uptake rates
are similar in many di€erent ecosystems, with daily
values ranging from 1 to 2 mg mÿ2 dayÿ1 (Born et al.,

0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved.

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S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

1990; Steudler et al., 1990; Yavitt et al., 1990; Mosier
et al., 1991). As Schimel et al. (1993) stated, we would
expect a wider range of soil oxidation rates if biotic
factors control methane consumption. Biotic limitations do occur with physiological water stress (Striegl
et al., 1992; Torn and Harte, 1996; Gulledge and Schimel, 1998b), but most data suggest that physical limitations on soil oxidation of methane dominate
methane oxidation.
Soil moisture is a factor that a€ects both physical
and biotic limitations of methane oxidation, and yet
few soil methane studies have experimentally reduced
soil moisture content in the ®eld to examine e€ects of
both water-®lled pore space and water bioavailability
on methane ¯uxes. This study examines the e€ects of
reduced soil moisture content on soil methane ¯uxes in
two forested sites. To evaluate e€ects of soil moisture

on the methane oxidation capacity of boreal forest
soils, we examined soil CH4 concentrations and CH4
uptake under altered and control precipitation regimes.
We assume soil CH4 uptake to be the net di€erence
between CH4 production and consumption by the soil.

2. Materials and methods
Soil atmosphere samples, CH4 ¯ux measurements,
and soil temperature and moisture data were collected
at two boreal sites with contrasting moisture regimes.
Data were collected throughout the 1996 and 1997
growing seasons at both an upland and a ¯oodplain
site. Both sites are located in the Bonanza Creek Long
Term Ecological Research site, 20 km southwest of
Fairbanks, Alaska (648N, 1488N). The mean annual
temperature is ÿ3.58C; the growing season is 90±100
days (van Cleve and Yarie, 1986). About 37% of
mean annual precipitation, 269 mm, is snow (Viereck
et al., 1993). Potential evapotranspiration is 466 mm
(Patric and Black, 1968). Snow cover generally is present from mid-October through April. Permafrost is

not present at either site.
The well-drained upland site is located on a ridge of
wind-deposited loess, 308 m above mean sea level. The
site is on a 258 slope, facing east±southeast. The soils
are Al®c Cryoquepts. Approximately 7 cm of decomposing litter overlies a rock-free, silt loam and silt subsoil. Paper birch (Betula papyrifera Marsh.), white
spruce (Picea glauca (Moench) Voss), and balsam
poplar (Populus balsamifera L.) are in the overstory
and total 2767 stems/ha. Dominant tree height is
about 18 m. It has been approximately 80 years since
the last forest ®re, the primary disturbance factor in
forests of this type.
The ¯oodplain site is about 10 km from the upland
forest, and is on poorly drained, alluvial Entisols,
classi®ed as Typic Cryo¯uvents. The top 25±30 cm of

the soil pro®le is silt loam, and from approximately 30
to 100 cm the pro®le is coarse sand. Several soil pits
contained 10±15 organic horizons from previous
¯oods, all within the top 100 cm. Litter depth on the
soil surface is about 9 cm. The site supports 780

stems/ha, comprising 40- to 50-year-old white spruce
reaching into an upper canopy of 100-year-old balsam
poplar. Dominant tree height is 20 m. A ¯ood was the
last major disturbance in this ecosystem, approximately 50 years ago. River terrace height is 3±3.5 m
above river water, and the site is 139 m above mean
sea level (Bonanza Creek Experimental Forest web
page, 1999). When the river level rises, the water table
can reach to 1 m below the soil surface.
At each site, a 0.10 ha, corrugated ®berglass shelter
is installed each May to limit summer precipitation
in®ltrating into the soil. These shelters have been
installed since 1989, and are removed each September
to allow a snowpack to accumulate. Soils receive
moisture input with snowmelt in the spring. All litter
accumulation from the shelter surface is spread over
the treatment area at the end of each growing season.
A moisture barrier of plastic sheeting is buried vertically 0.6 m deep around the perimeter of each shelter
to limit lateral moisture ¯ow into the treatment area.
Three replicate chambers and three replicate pro®les
existed both inside and outside of the shelters at both

sites.
Soil atmosphere CH4 concentrations were sampled
from tubing inserted into the ground at 20, 40 and 100
cm. Sampling locations were randomly picked inside
and outside the shelter. Nalgene plastic tubing, perforated at the ends to allow air ¯ow, was used at the 20
and 40 cm depths. The 100 cm depths have copper
tubing installed down to a 10 cm diameter, 30 cm long
PVC soil atmosphere reservoir. Flexible rubber tubing
was sealed to the tops of the sampling tubes with silicon. During the 1996 growing season, 10 ml syringe
samples were taken weekly at each 20, 40 and 100 cm
depth. Samples were taken at each depth every 2
weeks during 1997. At the upland site, samples were
also taken at 200 cm during the 1997 growing season.
Syringes were glass BDPack syringes with stopcocks
epoxied to the tips. Data from the 20 cm depth were
used to calculate methane ¯uxes into the soil from the
atmosphere. Shallower sampling wells were not
installed because of the 6±9 cm of organic horizon
overlying the mineral soil at both sites; we assumed
the zone of maximum oxidation to be within the top

10±20 cm of mineral soil (Whalen et al., 1992). Data
from depths deeper than 20 cm were used to examine
treatment e€ects on pro®le concentrations, and to see
if any methanotrophic or methanogenic activity at
these depths occurred that could a€ect the methane
concentration at 20 cm.
Soil methane uptake was measured at the same

S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

sampling locations as the CH4 pro®le concentrations,
each time pro®le samples were taken, using chamber
techniques. Plastic, 5.5 l containers with air-tight lids
were cut into the soil approximately 10 cm, adjacent
to the pro®le tubing. Chambers were 272.3 cm2 in
area. Syringe samples were taken from septa installed
in the lids, using the same type of syringe as for belowground atmosphere sampling. A sample of aboveground atmosphere was taken immediately adjacent to
the chamber to compare with the initial, time zero
sample inside the chamber. Subsequent samples were
taken at 15 and 30 min.

Samples were transported to a lab at the University
of Alaska Fairbanks and analyzed within 24±48 h. No
di€erence was found between samples immediately
analyzed and those analyzed after 3 days. Samples
were analyzed by a ¯ame ionization detector in a Shimadzu GC-14A gas chromatograph (Shimadzu,
Columbia, MD, USA), with a 2 m stainless steel column packed with Porapak Q. Standards were Scotty
gas standards (Scotty Gases, San Bernadino, California). We used the time-linear rate of decrease of CH4
in chambers in conjunction with chamber volume and
area to determine the rate of soil CH4 uptake.
Soil temperature was continuously recorded by thermistors (MK820, Siemens, Erlangen, Germany) connected to a datalogger (DL-2, Delta-T, Burwell, UK)
at 20, 40 and 100 cm depths, at locations inside and
outside the shelter corresponding to gas sampling locations. Soil volumetric moisture content (VMC) was
measured weekly using time domain re¯ectometry
(TDR, Tektronix, Beaverton, OR, USA) at two locations inside and two outside the shelters at 4, 10, 20
and 50 cm. VMC re¯ects the percentage water content
of the total soil volume. Soil water holding capacity
(WHC) was measured by saturating replicates of soil
samples from each gas sampling depth. Soil was then
allowed to drain for 24 h. Samples were weighed,
dried, and re-weighed for water content.

Attempts to predict soil methane uptake were made
using Fick's Law. This assumes that methane ¯ux is
primarily driven by di€usion gradients and not by temperature gradients. Fick's Law states that gas ¯ux J is
a function of the gas concentration gradient and the
gas di€usion coecient in free aboveground air:
J ˆ ÿDag


@C
@z

where J is methane ¯ux in g cmÿ2 sÿ1, Dag is the di€usion of methane in cm2 sÿ1 and @@Cz is the gas concentration gradient in ml lÿ1 across depths.
The value of D in a soil medium is an estimated
fraction of the known di€usion coecient in air, due
to tortuous path lengths and the moisture through
which soil gas must travel. Estimates of ¯ux calculated

1433

from Fick's Law are thus limited in accuracy by this
estimated value of D (Penman, 1940; Marshall, 1959;

Millington and Quirk, 1961; Currie, 1965; Rolston et
al., 1978), which is governed by constants particular to
the soil medium and the air-®lled porosity. Air-®lled
porosity was estimated from VMC and soil bulk density, which was determined using intact core samples,
according to Vomocil (1965). Fick's Law estimates are
also limited in accuracy by how dC=dz is calculated.
We used a form of Fick's Law used by Whalen et
al. (1992) at nearby, upland loessal sites in the
Bonanza Creek Experimental Forest, where soil properties were similar:
J ˆ 0:9
Dag
f 2:3


@C
@z

Dag is 0.194 cm2 sÿ1 and the constants 0.9 and 2.3 are
included to account for the tortuosity of the soil medium (Whalen et al., 1992; Campbell, 1985).
Statistical tests on the e€ects of the shelters were
performed using t-tests for equal means. When the
data were non-normally distributed, we used the nonparametric Wilcoxon rank-sum test. Signi®cance was
determined at a ˆ 0:05: Since our data were collected
from one rain-sheltered area at each site, these analyses compare a single set of treatment and control
soils at each ¯oodplain and upland locations. Results,
therefore, must be interpreted carefully, with an appreciation of the problems of pseudo-replication. We
assume for all tests that sheltered and unsheltered soils
were similar before rain-shelter installation.

3. Results
3.1. Soil moisture and temperature
The e€ect of the upland rainout shelters is most visible after rain events (Fig. 1). At the ¯oodplain, rainout shelters appreciably limited available soil moisture
throughout the summer (Fig. 1). Volumetric moisture
content (VMC) decreased with availability of water
from snowmelt under the shelter at each site. At the
upland site, VMC at 20 cm inside the shelters ranged
from 24 to 8% in 1996 and from 39 to 8% in 1997,
with higher values occurring immediately after snowmelt. Outside the shelters, the range was approximately
the same, but higher values occurred sporadically
throughout the growing season with precipitation
events.
VMC was much higher at the ¯oodplain site than at
the upland site. The water table at this site, sometimes
as shallow as 1 m below the forest ¯oor, ensured a
generally wetter soil environment than at the upland
site. Soil moisture at 20 cm ranged from 61 to 32%

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S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

inside and from 65 to 61% outside the shelter in 1996.
Values ranged from 50 to 28% inside and from 50 to
46% outside the shelter in 1997. During August 1997,
a ¯ooding event caused both sheltered and unsheltered
soil to increase in water content after minimum values
in early July.
Soil temperatures increased until August (July at the
¯oodplain in 1996) during both growing seasons
(Fig. 2). Small temperature di€erences were found
between locations inside and outside the rain-shelters
at each site. At the upland site, soil temperatures
underneath the shelter were consistently higher than
those outside in 1996. The di€erence was generally less
than 1.58C. The same trend was noted at the beginning
of the season in 1997. Temperatures under the shelter
were not recorded for part of this season. Soil temperatures at 20 cm ranged from 4 to 128C; in 1997 the
range was from 2 to 208C.
At the ¯oodplain site the shelter had the opposite
e€ect on soil temperature as that observed at the
upland; soil temperatures inside the shelter were consistently lower at 20 cm in 1996, for much of 1997
(Fig. 2) and throughout both growing seasons at 40

cm. The temperature di€erence was usually less than
28C. Temperatures at 20 cm in 1996 ranged from 0.5
to 78C; in 1997 they ranged from 1 to 7.88C. Soil temperatures were lower in 1996 at both sites; mean
monthly air temperatures during the growing season of
1996 ranged from 1 to 4.3, below those of 1997.

3.2. Soil pro®le CH4 concentrations
At the upland site, average methane concentrations
in the soil pro®le ranged from values close to atmospheric levels (at 20 cm) to a low of 0.29 ml lÿ1 at the
upland site at 100 cm. Pro®le methane concentrations
inside the shelter were signi®cantly lower than those
outside only at the 40 cm depth during 1996 and 1997
(P R 0.05). A signi®cant di€erence also was recorded
at the 200 cm depth in 1997 (P < 0.05).
At the ¯oodplain site, pro®le concentrations ranged
from close to atmospheric levels at 20 cm to a low of
0.40 ml lÿ1 at 100 cm. Concentrations inside the shelter
were signi®cantly higher than those outside at 20 and
40 cm depths in 1996 (P < 0.05).

Fig. 1. Volumetric soil moisture content at 10 and 20 cm in the soil pro®le at upland and ¯oodplain sites, 1996 and 1997. At the ¯oodplain site
in both years, data show a signi®cant di€erence between sheltered and unsheltered soil moisture. Upland di€erences in soil moisture are not signi®cant (P > 0.05).

S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

3.3. Rates of soil methane uptake
Average rates of soil uptake of methane at the
upland site ranged from 0.10 to 0.95 mg mÿ2 dayÿ1
(Fig. 3a). During both years, a signi®cant di€erence
was found between those rates measured inside and
those outside the shelter, with higher rates of methane
consumption occurring inside the shelter (P < 0.05).
At the ¯oodplain site, average rates of soil methane
uptake ranged from ÿ0.02 to 0.57 mg mÿ2dayÿ1
(Fig. 3b). Rates outside the shelter increased over the
summer of 1996. No such trend is visible during 1997,
when the rates were more varied both between
sampling locations and over the season. During 1996
rates of methane uptake were signi®cantly higher outside the shelter than inside (P < 0.05).

4. Discussion
4.1. Methane ¯uxes and soil pro®le methane
concentrations
Soil methane uptake rates at the upland site ranged
from 0.10 to 0.95 mg mÿ2dayÿ1 and were within the
range of those found at similar sites by Whalen et al.

1435

(1991) (see Fig. 3a). Floodplain rates had generally
lower values, ranging from ÿ0.02 to 0.57 mg
mÿ2dayÿ1 (Fig. 3b). Periodic methane release occurred
at this site. These uptake rates are low compared to
most rates recorded in temperate forests, but are
within the range of ¯ux rates reported in several studies (Steudler et al., 1989; Yavitt et al., 1990; King
and Adamsen, 1992; Dorr et al., 1993, Castro et al.,
1994; Hutsch et al., 1994; Schnell and King, 1994;
Bender and Conrad, 1995; Ambus and Christensen,
1995; Sitaula et al., 1995; Castro et al., 1995; Yavitt et
al., 1995). We expected lower rates of methane uptake
at the ¯oodplain site because of generally high soil
moisture there. For both summers, mean uptake rates
of methane in both sheltered and unsheltered areas at
the ¯oodplain were 0.16 2 0.02 mg mÿ2dayÿ1. At the
upland site, analogous mean rates were 0.4120.03 mg
mÿ2dayÿ1. The lower mean rates at the ¯oodplain site
suggest that high soil moisture may limit methane
uptake.
Some research indicates that limited soil water can
inhibit methane uptake. Torn and Harte (1996)
reported an optimum %WHC of 50% in temperate
montane soils, with oxidation becoming inhibited at
soil moisture levels below 20% moisture by weight.
Striegl et al. (1992) reported a positive relationship

Fig. 2. Soil temperature at 20 cm in the soil pro®le at upland and ¯oodplain sites, 1996 and 1997. P values result from a t-test for equal means.

1436

S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

between soil moisture and methane uptake in desert
soils. Many other studies report a negative relationship
between soil water content and methane consumption,
presumably because of di€usion limitations on
methane supply (King and Adamsen, 1992; Castro et
al., 1994; Castro et al., 1995; Sitaula et al., 1995; Whalen and Reeburgh, 1996). In a study on upland soils
supporting a white spruce forest in interior Alaska,
Gulledge and Schimel (1998b) found an optimum

moisture level of 30±40% of soil water holding capacity (%WHC) for soil methane oxidation rates in
the lab.
Our ®eld studies also suggest optimum moisture
levels for soil methane uptake. At the upland site,
where soil moisture is less than 20% by volume for
most of the growing season (Fig. 1), reducing water
availability signi®cantly increased methane uptake
rates (Fig. 3a). This suggests that the microbes were

Fig. 3. Methane ¯uxes into soil surface at upland (a) and ¯oodplain (b) sites, 1996 and 1997. P values are from t-tests for equal means. Error
bars are standard errors of the mean.

S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

limited in oxidation capacity by gas di€usion rates.
The soil at this site naturally was at or less than 28%
WHC for most of the two growing seasons of this
study, below the values suggested by Gulledge and
Schimel's (1998b) work for optimum methane uptake.
The increase of CH4 uptake rates under the shelter
suggests that being well-adapted to dry conditions
allowed the upland soil microbes to respond positively
to increased supplies of atmospheric methane, without
being negatively a€ected by the lack of moisture.
In comparison to the upland site, ¯oodplain
methane uptake data show the opposite response to
limited precipitation (Fig. 3b). Soil methane uptake
under the rain shelter, in spite of the reduction in
water-®lled pore space, was lower than at the unsheltered plots. The data suggest that the methane-consuming bacteria at this ¯oodplain site are so welladapted to volumetric soil moisture values of 60% and
higher (103% WHC) that reducing the water availability to 45% or lower (Fig. 1, 78% WHC) reduced
their ability to function, in spite of a presumed greater
ability of atmospheric methane to di€use into the soil.
Soil moisture values recorded at the ¯oodplain were
often far above the optimum of 30±40% WHC
reported by Gulledge and Schimel (1998b) for upland
boreal forest soils and yet many recorded uptake rates
at the ¯oodplain site were similar to those of the
upland soils.
The decrease in methane uptake under the ¯oodplain rain-shelter could also result from chemical
di€erences between precipitation and groundwater.
The treatment soils could be qualitatively di€erent
from the control soils in a way that is critical for
methanotrophic activity; soil pH, soil solution conductivity, or nutrient availability may have been altered in
a manner that limited methanotrophic activity, or that
fostered methanogenic activity. Another possibility is
that evaporative movement of soil water underneath
the shelter created a soil environment with too high a
salt concentration for methanotrophic activity. This
high salt environment as a result of soil water evaporation has been documented on ¯oodplain soils near
this site (Dyrness and van Cleve, 1993), though primarily at early succession sites.
A comparison of methane uptake by soils at both
upland and ¯oodplain sites suggests several possible
scenarios. Because we measured methane uptake and
not activity levels of methanotrophs and methanogens,
we need to consider possible responses of both populations. Populations of methanotrophic and methanogenic microbes in both ecosystems may be similar, but
may function di€erently because of the di€erent physical and chemical soil environment at the sites. Microbial population size and activity levels may also
di€er between sites as a result of di€erences in the soil
environment. Our study could also suggest that the

1437

soil microbial populations responsible for soil methane
oxidation and methanogenesis at the ¯oodplain site
may be composed of di€erent microbes than that at
the upland site. This scenario seems reasonable given
the suggestion in Gulledge et al. (1997) of physiologically distinct methane oxidizing populations at upland
sites of di€erent successional stages.
In spite of the assumed increased availability of atmospheric methane to the soil pro®le under the shelter,
there was no signi®cant di€erence between sheltered
and unsheltered methane pro®les at the upland site
depths of 20 cm. We presume this is due to either
increased methane consumption in the sur®cial layers
of the pro®le, or decreased methanogenesis. Data from
both summers also suggest that microbial methane
consumption increased, or methanogenesis decreased,
at 40 cm underneath the shelter; at this depth, the sheltered plots exhibited lowered methane concentrations.
We also found lower sheltered concentrations at 200
cm during the 1997 growing season. One possible explanation is spatially random sources of methane at
depths greater than 100 cm, providing substrate for
methanotrophic activity at these depths. On several occasions methane concentrations at 200 cm were higher
than those at 100 cm, ranging up to 1.62 ml lÿ1.
At the ¯oodplain site, the higher concentrations at
20 and 40 cm under the shelter correspond with the
lower methane uptake rates at these plots (Fig. 3b).
The increase in air-®lled pore space in the sheltered
soil allows more atmospheric methane to di€use into
the soil, but lowered consumption rates result in elevated concentrations. Although the 1997 data fall short
of signi®cance, a similar trend is evident as that in
1996.
4.2. Soil moisture, temperature and ¯ux relationships
Multivariate analysis of methane uptake rates with
soil moisture and temperature left much variability in
rates unexplained. Only one signi®cant model was
found, at the upland unsheltered sites in 1997 (P =
0.05, R 2 = 69), as a result of the strong relationship
with soil temperature (P < 0.05, R 2 = 0.64). Because
multivariate models in all other instances did not successfully predict our methane uptake rates, we examined soil moisture and temperature separately to try to
determine if and when they did a€ect ¯ux rates.
Although there were some signi®cant relationships
between soil moisture and methane ¯ux rates, at
both sites much of the variability in ¯ux was left
unexplained by soil water content. At the upland
site in 1996, there was a negative relationship
between soil moisture at 20 cm and the CH4 surface
¯ux rate (P < 0.05) underneath the shelter; soil moisture explained 55% of the variation in methane uptake.
That year, volumetric soil moisture varied from 8 to

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S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

24% from June through September. In 1997, we were
able to begin measurements sooner after snowmelt,
when volumetric soil moisture values were as high as
39%. Partially as a result of the low methane uptake
rates recorded at these high soil moisture values, both
the sheltered and the unsheltered plots have signi®cant,
negative relationships between soil water and methane
consumption in 1997, explaining 64 and 60%, respectively of the variation in uptake rates.
At the ¯oodplain site, the sheltered sites show little relationship between soil moisture at 20 cm and
methane uptake rates. Outside the shelter in 1996, a
negative relationship was established, with soil
moisture explaining 51% of the variation in uptake
rates, all at moisture values above 60% (P < 0.05).
Outside the shelter at the ¯oodplain site in 1997, two
points representing the lowest rates were leverage
points in a signi®cant, positive relationship between
moisture and methane uptake rates. One of these
points most likely represents a pulse of methane production, as there was net e‚ux inside a chamber. The
other point was the ®rst data point of the season,
when methane uptake was negligible and moisture
availability was low because of freezing soil temperatures.
Soil temperature was also not a good predictor
of methane ¯ux. This corresponds to a study by
Castro et al. (1993). At both sites, lower uptake
rates generally occurred at the beginning of the season when soil moisture was high and soil temperatures were low. However, there was only one
positive, signi®cant relationship between methane
consumption and soil temperature at 20 cm, at the
upland unsheltered plots in 1997 (P < 0.05, R 2 =
0.64). The increase in methane uptake rates for this
one signi®cant relationship occurred at soil temperatures above 108C; Castro et al. (1995) suggested that
temperature had a positive e€ect on methane consumption between ÿ5 and 108C and no e€ect between
10 and 208C. Also contrasting with our results, Crill
(1991) reported a strong temperature response in early
spring and a lessened e€ect during the summer.
Because of the generally non-signi®cant relationships
between methane uptake and soil temperature at our
sites, we assume that the small soil temperature di€erences resulting from the rain-shelters had a negligible
e€ect on uptake rates; soil temperature di€erences may
have been more pronounced nearer the soil surface,
however.
The lack of a signi®cant relationship between soil
temperature and methane ¯ux at most plots suggests
that soil physical parameters may be more in¯uential
determinants of methane ¯ux. This is consistent with
several other studies of soils functioning as a CH4 sink
(Torn and Harte, 1996; Whalen and Reeburgh, 1996;
Born et al., 1990). To more closely examine concepts

of physical limitations on soil CH4 uptake, we used
Fick's Law to predict soil CH4 ¯uxes.

4.3. Fick's Law predictions
Many studies have used Fick's Law to calculate
¯uxes of various gases into and out of the soil surface
(Table 1). Fick's Law represents gaseous mass ¯ux
across a horizontal plane. The ability of Fick's Law to
estimate gas ¯uxes at the soil surface plane depends on
several conditions:
1. dC=dz measurements at depth z must be close
enough to the soil surface for the concentration gradient to re¯ect the concentration gradient immediately below the soil surface. This is violated at
depths commonly used for measurements of dC=dz
such as 10 or 20 cm (Yavitt et al., 1990).
2. Alterations to D accounting for soil tortuosity must
account for heterogeneous soil conditions (Rolston
et al., 1978). Heterogeneous quantities of roots, root
channels, moisture variability and organic matter all
limit the accuracy of tortuosity coecients.
3. Gas consumption or production within the pro®le
depth from which ¯uxes are calculated must be negligible. This is true in the case of biologically inert
gases such as radon (Dorr and Munnich, 1990);
CH4 can be both produced and consumed by biological processes in a given soil pro®le, especially
near the ground surface.
Because of these conditions, most calculations of
soil gas ¯ux represent ¯uxes within the soil pro®le, qz ,
rather than the surface ¯ux, q0 : If the concentration of
CH4 decreased linearly with depth through the top 20
cm soil, we assume that the concentration gradient we
measured from 20 cm to the atmosphere immediately
above the soil surface re¯ects the gradient across a
plane with a midpoint in this soil compartment at z =
10 cm. Thus our Fick's Law calculations more likely
represent the ¯ux of gas across this plane …qz † and not
the soil surface ¯ux …q0 ). The calculations must be considered estimations because of studies suggesting that
CH4 concentrations do not decrease linearly with
depth (Whalen et al., 1992; Yavitt et al., 1990).
Calculations of qz cannot be expected to corroborate
with measurements of q0 because of microbial consumption and production of CH4 at these shallow
depths in the soil pro®le. The conservation of mass (de
Jong and Schappert, 1972; Striegl 1993) explains how
biological sources or sinks of CH4 a€ect the relation
of qz to q0. The one-dimensional continuity equation
states that the change in gas concentration over time
… @@Ct † at any point is the change in ¯ux … @@ qz †, plus any
sources or sinks produced or consumed at that point
(S ). Hence,

1439

S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

Table 1
Studies using Fick's Law to calculate ¯ux rates of various gases at the soil surface, estimations of di€usion coecient (if available), estimation of
dC/dz, and results of any comparison to measured ¯uxes. Soil taxa given when provided in study
Soil system

Estimate of D

Global

D/D0 from Millington 0.04 ppmv cmÿ1
and Shearer (1971)
(a) Flux measured in
Slope of gradient to 20 cm
cores to derive D
(b) 0:9
D
f 2:3 , D
cm2sÿ1
0:9
D
f 2:3 , D cm2sÿ1 Unspeci®ed for calculations,
measured at various depths

Agricultural soil, Ottawa, Canada

New York state hardwood forest

Agricultural loamy sand
(Psammentic Hapludalf) Ontario,
Canada
Alpine, sub-alpine Wyoming

Boreal forest, Alaska
Appalachian mountains, West
Virginia

Estimate of dC/dz

Authors

No

Potter et al.
(1996)
Dun®eld et al.
(1995)

Yes; both methods within 3.8
mmol mÿ2 dayÿ1 of measured CH4
¯uxes, 19.1±23.9 mmol mÿ2dayÿ1
Yes; Fick's law overestimated
except in early spring (see
reference)
No

Yavitt et al.
(1995)

1:3
D
f1:7 , D m2sÿ1

Unspeci®ed for calculations,
measured at various depths

0.139 cm2 sÿ1 CO2,
N2O; 0.22 cm2 s ÿ1
CH4
0:9
D
f 2:3 , D cm2
sÿ1
0.186 cm2 sÿ1,
Marrero and Mason
(1972)

Average gradient from 100
cm in snowpack

No

Slope of gradient to 20 cm

Yes; calculations were higher than Whalen et al.
static chamber measured ¯uxes
(1992)
Yes; similar to ¯uxes in cores
Yavitt et al.
(1990)

Unspeci®ed for calculations,
measured at various depths

@C
@q
ˆ
‡S
@t
@z
Integrating over the depth pro®le [0, z ], the depthaveraged equation becomes:
z


Comparison with measurements

@C
ˆ q0 ÿ qz ‡ z
S
@t

where q0 is ¯ux at the soil surface plane and qz is ¯ux
across the plane at depth z. Thus the only way q0
(measured surface ¯ux) can equal qz (calculated Fick-

Burton and
Beauchamp
(1994)
Sommerfeld et
al. (1993)

ian ¯ux) is if z
S and z
@@Ct are the same, meaning
that the source or sink of CH4 in the soil pro®le compartment must exactly equal the change in depth-averaged concentration with time. Since q0 was measured
over 30 min intervals, we assume that @@Ct 10; consequently, any di€erence between q0 and qz is only due
to S. Because signi®cant CH4 oxidation capacity can
be concentrated near 10 cm in the soil pro®le (Whalen
et al., 1992; Gulledge et al., 1996), S can be a signi®cant factor in the equation.

Fig. 4. Calculated …qz † vs. measured (qo) soil CH4 ¯ux rates at upland and ¯oodplain sites, 1996 and 1997. Perfect correspondence between calculated and measured ¯uxes would fall on the one-to-one line in each graph.

1440

S.A. Billings et al. / Soil Biology & Biochemistry 32 (2000) 1431±1441

Fick's Law predictions of qz were signi®cantly related to the observed CH4 ¯ux (q0) at the sheltered
upland plots during 1997 (Fig. 4). At all other locations during 1997 and at both the upland and ¯oodplain sites during 1996, both sinks and sources of CH4
in the top 10 cm of the soil pro®le prevented qz from
being signi®cantly related to measured surface ¯ux, q0.
The varying e€ects of soil moisture on both methanotrophy and methanogenesis were particularly evident
at the ¯oodplain plots, where qz often was lower than
q0 : Our work with Fick's Law indicates that the sink
term for methane in the top layers of these soil pro®les
can overwhelm calculations of ¯ux estimates.

5. Conclusions
If we assume treatment and control soils were similar before installation of the rain-shelters, the contrasting responses of soil CH4 uptake to summer rainfall
exclusion at these sites suggest several possible scenarios. Forests with some tree species in common, but
di€erent soil chemical and physical environments, may
support di€erent population sizes of methanogenic and
methanotrophic microbes, di€erent species of microbes, or varied levels of soil microbial activity. This
knowledge is critical for predicting the forest soil sink
for atmospheric methane on a landscape level, particularly for modelers who may use broad classi®cation
schemes to de®ne forest types.

Acknowledgements
This work was supported by a NASA Earth System
Science Global Change Fellowship. Many thanks go
to the sta€ of the Bonanza Creek Experimental Forest
and the University of Alaska Fairbanks. Dr. Richard
Boone generously provided lab space and equipment.
Dr. Steve Whalen was generous with his time, equipment and helpful commentary. Drs. Jay Gulledge and
Gabriel Katul provided insightful discussions.

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