Low-Temperature Respiration
in Arctic Soils
G.J. Michaelson and C.L. Ping
University of Alaska Fairbanks,
School of Natural Res. and Agric. Sciences
SUMMARY
With fall snow cover, cold-season soil temperatures in arctic soils hover around
0oC for an extended period during the early winter and then as soil bulk water
freezes, soil temperatures drop to subzero levels. Soil respiration under
conditions representing these two phases of the cold-season was studied using
cryobath incubation experiments at 0oC and –2oC. The study included a total of
98 fresh-frozen soils from the ATLAS and LAII flux study sites along the
western Alaska transect and from the Kuparuk River Basin transect extending
from Prudhoe Bay to Toolik Lake. Organic surface horizons [O-horizons]
respired at average rates 2.5 times higher than mineral horizons at both
temperatures. Results indicate that as bulk soil water freezes, respiration rates
fall an average of 91% in tundra O-horizons and 70% in corresponding
shrub/forest soils, as compared to 85% in mineral horizons. At 0oC before bulk
soil water freezes, soil respiration rates were more closely related to soil watersoluble organic carbon [OCws] stocks in O-horizons and to soil total organic
carbon [TOC] stocks for mineral horizons. As bulk soil water freezes at –2oC
these apparently different associations for organic and mineral horizons were
strengthened. While OCws stocks are good predictors of respiration in the
surface O-horizons, soil TOC stocks are better than OCws as predictors of lowtemperature respiration for mineral horizons. These data indicate that with
information on soils and soil organic carbon contents, it should be possible to
predict CO2-respiration responses of arctic soils under changed winter-season
conditions.
Introduction
It has been found that respiration in arctic soils can continue until soil
temperatures drop to –10oC or lower [Flanagan and Veum, 1974]. Significant
amounts of CO2 gas flux have been observed during the cold-season, and it is
estimated that this can account for up to 60-80% of the net ecosystem exchange
[Oechel et al., 1997]. High CO2-efflux rates have been observed particularly
during the shoulder-seasons around September-October-November and again in
May. Soil temperatures in the active layer during these months are often nearly
isothermal at around 0oC [see example, Figure 1]. The duration of these periods
of moderately cold temperatures is highly dependent on seasonal snow
conditions and air temperature, and thus there is considerable inter-annual
variation. With climate change over a decadal time-period, changes in average
duration of these isothermal periods could have significant effects in net
ecosystem function and C-dynamics.
Soil temperature during the cold-season can be divided with regard to the
physical state of bulk soil water i.e. frozen or unfrozen [Figure 1]. Soil
temperatures remain at or near 0oC when bulk soil water is cooled but still in a
liquid state and then as temperatures drop below 0oC, bulk soil water freezes
leaving only brine-films around soil particles. Presumably soil biological
respiration must occur in a liquid water medium, therefore at the time when soil
bulk water freezes there should be a major impact on soil respiration. At this
point of freezing there is a drastic change in the amount of soil liquid water. It
follows at there should also be a change in the access to and availability of soil
organic matter [SOM] as substrates for soil respiration. In order to understand
and predict cold-season respiration activity, more must be known about the
factors controlling respiration across this major dividing point in soil water and
temperature conditions as it occurs twice a year at onset and conclusion of the
cold-season.
Objectives
This study was undertaken to investigate cold-season soil respiration and the
interaction of soils and SOM substrates with temperature, as bulk soil water
freezes under cold-season soil conditions. The three main questions were:
1. How do soil respiration rates vary across the threshold temperature of 0oC
below which most of bulk soil water freezes?
2. Does soil respiration rate respond to temperature drop across the OoC mark
with different sensitivity in surface organic soils compared with mineral
subsurface soil?
3. When bulk soil water freezes, is there an apparent change in the SOM
substrates important for respiration such that water-soluble substrates
become more closely related to observed soil respiration rates?
Laboratory Study Methods
Soils and Incubations – Samples were collected from the genetic horizons
representing the active layers (or upper 1 meter) at the LAII-ATLAS C-flux
study sites at Oumalik, Ivotuk, Council, Mauze Creek, and at Kougarok in
western Alaska and at the LAII-Flux sites at Betty Pingo, Deadhorse, Sagwon,
Happy Valley and Toolik [Figure 2]. Samples were kept frozen at –15oC and at
field moisture content until just before incubations began. Two separate sets of
98 soil samples were incubated in constant temperature cryobaths [see Figure
3], one at 0oC and another at –2oC. Samples were incubated in 250 cm3 jars
containing 150 cm3 cores packed to the field-bulk densities for individual soil.
Carbon dioxide respiration rates were measured weekly using a Columbus
Instruments Mico-oxymax respirometer and the 2-week rates used for this study.
Soil Characteristics – Soil moisture contents were determined on parallel
samples taken at incubation, one to represent 0oC water content by oven-drying
at 105oC and one at –2oC by Vitel sensors placed in incubated samples. Total
OC was determined on a LECO 1000 CHN Analyzer. Soil water-soluble
organic carbon [OCws] was indexed by determination of the dissolved organic
carbon in solution [.45 m filtered] after a 4 hr. equilibration at 25oC using 150
cm3 of thawed field-moist soil with an equal volume of deionized water. Organic
horizons had TOC contents of >20% while mineral soils were 20% TOC.
Toolik Lake, Alaska 2000
Much of Active Layer @ 0oC
0oC
Active Layer < 0oC
0oC
< 0oC
Figure 1. An example of the annual soil temperature cycle [R. F.
Paetzold, C.L. Ping and V.E. Romanovsky, unpublished
data].
Figure 3. Cryobath incubations and respirometer.
Results
Respiration Rates [Table 1]

Unfrozen water content at 0oC averages higher [66%] as would be
expected in organic horizons [O-horizons] compared to mineral horizons
[31%]. At –2oC much of soil bulk water freezes and average unfrozen
water contents fall to about the same level [6-7%] for both Organic and
mineral horizons. However, O-horizons lose about 90% of their liquid
water compared to only an average 77% for mineral horizons. There is no
apparent direct or simple relationship between soil liquid water and
respiration rate.

Respiration rates at both temperatures averaged higher in organic
compared to mineral horizons.

O-horizons from tundra sites had the highest average respiration rates
at 0oC but their rates were more sensitive to temperature or freezing of soil
bulk water than organics from shrub and forest sites. As temperature
dropped from 0oC to –2oC, respiration in tundra organic soils fell 90-92%,
while respiration in the shrub and forest O-horizons fell only 62-75%. At –
2oC O-horizons from shrub and forest sites had average respiration rates
almost twice as high as corresponding soils from tundra sites.

Mineral horizons from the group including permafrost, lichen cover, or
nonacidic tundra sites, and the group of Bg horizons, each had respiration
rates that averaged highest among mineral horizons at both temperatures.
The Council B-horizons respired at lower rates than most mineral horizons.
Soil OC and Respiration [Table 2]
Organic Horizons

Respiration rates in O-horizons were more closely related to OCws
than TOC at both temperatures. Relationships between respiration and
OCws were improved with dropping temperature. The only significant
relationship for respiration and TOC among O-horizons was for the Council
forest sites and this was only due to a high negative correlation [r=-0.85]
between TOC and OCws among those soils. The forest surface O-horizons
are less dense and high in OCws [and respiration] but are lower in TOC
compared with the denser more decomposed O-horizons immediately below
them [forest Oi versus Oa horizons respectively].

As data are grouped by site or vegetative-cover within site,
relationships improve [Figure 4]. Respiration in O-horizons from shrub
and forest sites was very highly related to OCws at –2oC [R2=0.90-0.97] and
at OoC but with more scatter in data. However, respiration responds
differently in forest organic soils and any significant relationship between
respiration and OCws is lost at 0oC.
Mineral Horizons

When all mineral horizons were grouped together, respiration was not
related to OCws and only weakly related to TOC [Table 2, and Figure 5].
Data grouped by soil horizon type and site vegetative cover improved some
relationships.

Respiration rates were not related to OCws or TOC for the Bw or Bg
all-inclusive groups, but when B-horizons from these were selected for their
close proximity to the surface O-horizons, TOC was highly related to
respiration at 0oC [R2=0.86]. Stocks of OCws were low and –2oC
respiration rates low for this group [Table 1] and there were no significant
relationships for OCws or TOC.

The Bf/Lichen/NATundra-group had the highest overall respiration
rates [Table 1]. In this group, OCws and TOC were significantly correlated
with each other [r=0.73, p<0.01]. Therefore, respiration at –2oC was
significantly related to both OCws and TOC [Table 2] but only TOC
related to respiration at 0oC.

Respiration at –2oC in mineral B-horizons from Council forests was
highly related to TOC but the relationship was significantly reduced at 0oC.
Conclusions
1. As soil bulk water freezes, respiration in soil surface O-horizons of arctic
Alaska can be expected to drop [on average 86% in this study]. During the
early cold-season when soil temperatures are at 0oC, tundra organic layers
are respiring at higher general rates than shrub and forest organic layers.
But as bulk soil water freezes, respiration rates in tundra organic layers
will drop more drastically than those of the shrub and forest soils and be
respiring at rates averaging approximately half that of the shrub and forest
soils.
2. As soil temperature drops from 0oC to –2oC, soil respiration in mineral
horizons can be expected to drop on average about the same as for the
surface O-horizons [about 85%]. Overall respiration response to
temperature is less variable among mineral horizons compared with Ohorizons.
3. Respiration rates in O-horizons relate reasonably well to index soil stock
levels of soil water-soluble organic carbon (OCws), this relationship is
especially strong at subzero temperatures after bulk soil water has frozen.
Mineral horizons however, appear to be more complex and apparently a
variety of factors are significant in determining respiration rates at low
temperatures. However, low-temperature respiration related reasonably
well to total organic carbon [TOC] present for groups such as those
mineral horizons close to the surface, those associated with higher levels of
activity [i.e. permafrost, lichen, and nonacidic tundra associated mineral
horizons], and those found in more specific locations or groups as under
forest at Council.
4. Given the apparent strength of the relationships between CO2-respiration
and either OCws or TOC stocks it seems that prediction of soil respiration
responses under changed cold-season soil temperature conditions should be
possible as an aid in modeling winter CO2-fluxes. These results point to
the importance of soil temperature and snow-cover on the duration of the
0oC soil isothermal period and its potential for significant impacts to coldseason CO2-fluxes from arctic soils.
Acknowledgements:
The authors wish to thank Vladimir Romanovsky for his assistance with
measurement of soil unfrozen water content and the Palmer AFES-Laboratory
for soil chemical analysis.
References
Flanagan, P. W., and A.K. Veum, Relationship between respiration, weight loss,
temperature and moisture in organic residues on tundra, in Soil Organisms and
Decomposition in Tundra, edited by A.J. Holding, O.W. Heal, S.F. MacClean
Jr., and P.W. Flanagan, pp. 249-277, IBP Tundra Biome Steering Committee,
Stockholm, Sweden, 1974.
Oechel, W. C., G. Vourlitis, and S.J. Hastings, Cold season CO2 emission from
arctic soils, Global Biogeochem. Cycles, 11, (2), 163-172, 1997.
Table 1. Selected data averages for 98 study soils (37 organic and 61 mineral horizons).
Unfrozen Water
Soil Horizon Type
Group by Site or Veg.
Resp. Rate
OCws
n
0oC -2oC
Vol. %
0 to-2oC
TOC
0oC
g m-2 cm-1
-2oC Change
gCO2 cm-3 da-1
%
Organic
Tundra (All)
Tundra (Acidic)
Shrub (All)
Shrub (Council)
Forest (Council)
37
25
12
8
5
4
66
70
75
54
68
63
6
7
7
5
7
6
2.0
1.8
1.8
2.1
2.7
2.5
680
730
740
470
620
640
57.3 8.3
60.8 6.3
66.0 5.3
44.5 11.0
35.3 13.3
47.7 13.0
-86
-90
-92
-75
-62
-73
Mineral
Bg
Bw
B-hor. (near surface)1
Bf, Lichen, NATundra2
B-hor. (Council )
61
10
26
11
13
8
31
27
27
29
37
42
7
7
5
8
9
10
0.74
0.86
0.81
0.46
0.78
0.30
500
770
500
390
450
300
22.0
27.6
18.8
18.1
27.8
14.8
-85
-87
-88
-86
-80
-83
1
2
B-horizons immediately beneath surface organic horizons.
B –horizons of permafrost (Bf), from lichen vegetated sites, and from nonacidic tundra sites (NAT).
3.3
3.6
2.3
2.6
5.6
2.5
Table 2. Regression coefficients (R2) for respiration rate as a
function of water-soluble organic carbon index (OCws) and total
organic carbon (TOC).
1
n
OCws
0oC
-2oC
0oC
Organic
Tundra (All)
Tundra (Acidic)
Shrub (All)
Shrub (Council)
Forest (Council)
37
25
12
8
5
4
0.21**
0.32**
0.50**
0.64*
0.93***
0.11
0.69***
0.45***
0.64**
0.90***
0.96***
0.97***
0.03
0.01
0.02
0.10
0.09
0.02
0.15
0.14
0.01
0.14
0.03
0.84***
Mineral
Bg
Bw
B-hor. (near surface)1
Bf,Lichen, NATundra2
B-hor. (Council)
61
10
26
11
13
8
0.15
0.14
0.19
0.18
0.11
0.01
0.04
0.01
0.01
0.01
0.73***
0.02
0.23***
0.15
0.05
0.86***
0.60**
0.45*
0.29***
0.02
0.01
0.06
0.69***
0.86***
Soil Horizon Type
Group by Site or Veg.
TOC
-2oC
B-horizons immediately beneath surface organic horizons.
B –horizons of permafrost (Bf), from lichen vegetated sites, and from nonacidic tundra sites (NAT).
***, **, * F-test of regression significant at the p>0.001, 0.01, and 0.10 levels respectively.
2
Organic Horizons
0C
250
y = 0.19x + 20.6
R2 = 0.21
200
150
100
50
0
0
100
200
300
g wsOC cm-3
-1
o
30
-3
300
25
Respiration gCO2 cm da
Respiration gCO2 cm-3 da-1
All
400
-2oC
y = 0.06x - 1.3
R2 = 0.69 p>.001
20
15
10
5
0
500
0
100
200
300
g wsOC cm-3
400
500
300
Respiration gCO2 cm-3 da-1
Respiration gCO2 cm-3 da-1
Tundra (Acidic)
o
0C
y = 0.43x + 3.1
250
2
R = 0.50 p>.01
200
150
100
50
0
0
100
200
300 -3 400
g wsOC cm
30
-2oC
25
y = 0.06x - 1.78
2
R = 0.64 p>.01
20
15
10
5
0
500
Shrub (all)
0
100
200
300
g wsOC cm-3
400
500
120
Respiration gCO2 cm-3 da-1
Respiration gCO2 cm-3 da-1
Shrub (all)
o
0C
100
y = 0.27x - 14.6
R2 = 0.64 p>.10
80
60
40
20
0
0
100
200
300
g wsOC cm-3
25
o
-2 C
20
y = 0.06x - 1.94
R2 = 0.90 p>.001
15
10
5
0
0
400
100
200
300
g wsOC cm-3
400
60
Respiration gCO2 cm-3 da-1
Respiration gCO2 cm-3 da-1
Forest (Council)
o
0C
50
40
30
y = 0.016x + 43.8
R2 = 0.11
20
10
0
0
100
200
300
g wsOC cm-3
400
500
25
-2oC
20
15
y = 0.047x + 1.73
R2 = 0.97 p>.001
10
5
0
0
100
200
300
g wsOC cm-3
400
500
Figure 4. Soil water-soluble organic carbon [OCws] and soil
respiration for selected groups of organic soil
horizons.
Mineral Horizons
150
Respiration gCO2 cm-3 da-1
Respiration gCO2 cm-3 da-1
All
o
0C
y = 0.36x + 4.39
100
2
R = 0.23 p>.001
50
0
0
50
100
150
-3
mg TOC cm
30
-2oC
25
y = 0.078x - 0.53
R2 = 0.29 p>.001
20
15
10
5
0
0
200
50
100
150
-3
mg TOC cm
200
40
35
30
25
20
15
10
5
0
Respiration gCO2 cm-3 da-1
Respiration gCO2 cm-3 da-1
B-hor. (near surface)
o
0C
y = 1.32x - 30.7
R2 = 0.86 p>.001
0
10
20
30
40
mgTOC cm-3
50
60
10
-2oC
8
y = -0.073x + 5.30
2
6
R = 0.06
4
2
0
0
10
Bf, Lichen, NATundra
20
30
40
mgTOC cm-3
50
60
100
Respiration gCO2 cm-3 da-1
Respiration gCO2 cm-3 da-1
Bf, Lichen, NATundra
o
0C
80
60
y = 0.40x + 6.21
2
R = 0.60 p>..01
40
20
0
0
50
100
150
mgTOC cm-3
30
o
-2 C
y = 0.15x - 2.33
R2 = 0.69 p>..001
20
10
0
200
0
50
100
150
mgTOC cm-3
200
35
30
25
20
15
10
5
0
Respiration gCO2 cm-3 da-1
Respiration gCO2 cm-3 da-1
B-hor. (Council)
o
0C
y = 0.41x + 3.32
R2 = 0.45 p>.10
0
10
20
30
40
-3
mgTOC cm
50
60
6
o
-2 C
y = 0.10x - 0.38
5
R2 = 0.86 p>.001
4
3
2
1
0
0
10
20
30
40
-3
mgTOC cm
50
60
Figure 5. Soil total organic carbon [TOC] and respiration for
selected groups of mineral soils.