Tree Physiology 23, 273–280
© 2003 Heron Publishing—Victoria, Canada
Field measurements of root respiration indicate little to no seasonal
temperature acclimation for sugar maple and red pine
ANDREW J. BURTON1,2 and KURT S. PREGITZER1,3
1
School of Forestry and Wood Products, Michigan Technological University, Houghton, MI 49931, USA
2
Author to whom correspondence should be addressed ([email protected])
3
USDA Forest Service, North Central Research Station, Houghton, MI 49931, USA
Summary Increasing global temperatures could potentially
cause large increases in root respiration and associated soil
CO2 efflux. However, if root respiration acclimates to higher
temperatures, increases in soil CO2 efflux from this source
would be much less. Throughout the snow-free season, we
measured fine root respiration in the field at ambient soil temperature in a sugar maple (Acer saccharum Marsh.) forest and a
red pine (Pinus resinosa Ait.) plantation in Michigan. The
objectives were to determine effects of soil temperature, soil
water availability and experimental N additions on root respiration rates, and to test for temperature acclimation in response
to seasonal changes in soil temperature. Soil temperature and
soil water availability were important predictors of root respiration and together explained 76% of the variation in root respiration rates in the red pine plantation and 71% of the
variation in the sugar maple forest. Root N concentration explained an additional 6% of the variation in the sugar maple
trees. Experimental N additions did not affect root respiration
rates at either site. From April to November, root respiration
rates measured in the field increased exponentially with increasing soil temperature. For sugar maple, long-term Q10 values calculated from the field data were slightly, but not
significantly, less than short-term Q10 values determined for instantaneous temperature series conducted in the laboratory
(2.4 versus 2.6–2.7). For red pine, long-term and short-term
Q10 values were similar (3.0 versus 3.0). Sugar maple root respiration rates at constant reference temperatures of 6, 18 and
24 °C were measured in the laboratory at various times during
the year when field soil temperatures varied from 0.4 to
16.8 °C. No relationship existed between ambient soil temperature just before sampling and root respiration rates at 6 and
18 °C (P = 0.37 and 0.86, respectively), and only a very weak
relationship was found between ambient soil temperature and
root respiration at 24 °C (P = 0.08, slope = –0.09). We conclude that root respiration in these species undergoes little, if
any, acclimation to seasonal changes in soil temperature.
Keywords: Acer saccharum, N additions, Pinus resinosa, Q10,
soil moisture, soil temperature.
Introduction
Root respiration often comprises from one third to more than
one half of total soil CO2 efflux in forest ecosystems (Edwards
and Harris 1977, Nakane et al. 1983, Behera et al. 1990,
Bowden et al. 1993). If root respiration rates increase rapidly
with temperature, as would be predicted from typical Q10 values of 2 or greater, higher temperatures could cause large increases in root respiration and associated soil CO2 efflux
(Boone et al. 1998). However, if root respiration acclimates to
temperature, increases in soil CO2 efflux due to climate warming might be small.
Temperature acclimation has been commonly reported for
dark respiration of foliage (Rook 1969, Sorensen and Ferrell
1973, Teskey and Will 1999, Tjoelker et al. 1999a, 1999b,
Atkin et al. 2000b, Gunderson et al. 2000, Will 2000), and
mechanisms that could account for an acclimation response
have been proposed. Changes in adenylate control (turnover
of ATP to ADP) of respiration could occur in association with
an altered demand for ATP or a change in the activity of the
nonphosphorylating alternative pathway. Variation in soluble
carbohydrate concentrations could also cause acclimation by
altering substrate availability or respiratory gene expression,
or both (Atkin et al. 2000a). However, the actual mechanisms
underlying temperature acclimation of respiration remain unclear, and the degree of acclimation can vary widely from
complete acclimation, or homeostasis, to slight or nonexistent
(Larigauderie and Körner 1995). Nevertheless, for many
plants, acclimation of foliar dark respiration can result in CO2
losses in a warmer environment that are significantly less than
would be predicted from instantaneous temperature response
curves (Larigauderie and Körner 1995, Tjoelker et al. 1999a).
Less is known about temperature acclimation of root respiration, but it has been observed in roots of seedlings in the laboratory (Bryla et al. 1997, 2001, Tjoelker et al. 1999a), and in
young citrus trees (Bryla et al. 2001) and grass species in the
field (Fitter et al. 1998). In contrast, temperature acclimation
of root respiration was not observed in small Picea
engelmannii Parry or Abies lasiocarpa (Hook.) Nutt. trees
(Sowell and Spomer 1986), or in roots of Picea glauca
(Moench) Voss seedlings (Weger and Guy 1991). To our
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Received March 28, 2002; accepted September 13, 2002; published online February 3, 2003
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BURTON AND PREGITZER
Materials and methods
Study sites
The study sites were a 90-year-old second-growth sugar maple
forest and a 50-year-old red pine plantation in Michigan’s Upper Peninsula. The sugar maple forest had a basal area of 35 m2
ha –1, of which 90% was sugar maple. The red pine plantation
had a basal area of 34 m2 ha –1 comprised entirely of red pine.
Each study site contained six 30 m × 30 m study plots, three of
which were control plots and three of which received N additions. At the sugar maple site, 30 kg N ha –1 as NaNO3 was
added in six 5-kg increments per year beginning in 1994. At
the red pine site, 100 kg N ha –1 was added in four 25-kg increments per year beginning in 1998. The red pine plantation had
virtually no understory or ground vegetation. In the sugar maple forest, the sapling and seedling layers had sugar maple
dominance similar to that occurring in the overstory. Thus fine
roots sampled for respiration contained virtually no roots other
than those of the study species.
Soil temperature and matric potential were continuously
monitored at the sites. In all plots, soil moisture blocks (Model
5201, SoilMoisture Equipment, Santa Barbara, CA) were
placed at a depth of 15 cm, and temperature thermistors
(Model ES-060-SW, Data Loggers) were placed at 5 and
15 cm. Moisture blocks and thermistors were read every
30 min by data loggers (EasyLogger Models 824 and 925,
Data Loggers, Logan, UT), with mean values recorded every
3 h. Moisture block resistance readings (ohms) were converted to matric potential (MPa) based on relationships developed in the laboratory from moisture blocks placed in intact
soil cores collected from the plots and equilibrated on soil
moisture plates at potentials ranging from –0.01 to –1.5 MPa.
In 1999, soil temperature profiles were also measured at each
site with thermistors (Model TMC6-HB, Onset Computer,
Bourne, MA) placed at 1, 5, 10 and 20 cm, with data recorded
every 30 min by data loggers (Model H8 4-Channel External,
Onset Computer).
Field root respiration at ambient soil temperature
During the 1998 and 1999 growing seasons, root respiration
rates were measured in the field at ambient soil temperature 17
times at the sugar maple site and 9 times at the red pine plantation. Root respiration measurement dates included the months
April through November at the sugar maple site and June
through November at the red pine plantation. On the measurement dates, soil temperature at 5-cm depth ranged from 4.3 to
19.2 °C in the sugar maple forest and from 5.3 to 20.9 °C in the
red pine plantation. Samples for field measurements of root
respiration consisted of a bulked sample of fine roots (≤ 1 mm
diameter) collected from the top 5 cm of organic matter and
mineral soil at three to four locations within each plot. At these
soil depths, soil temperature is well coupled to dynamic
changes in air temperature (Brown et al. 2000). A trowel was
used to overturn a small area (about 10 cm × 10 cm) of surface
soil at each location from which root samples were collected.
The roots were brushed free of loose soil and organic matter,
but were not washed or rinsed. Root samples typically con-
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knowledge, respiratory temperature acclimation has not been
assessed in roots of mature trees in natural ecosystems.
The possible existence of temperature acclimation of root
respiration has a variety of implications. If root respiration acclimates to seasonal changes in temperature, as has been observed for foliar dark respiration (Pereira et al. 1986), then
estimates of annual root respiration fluxes based on temperature response curves made at one point in time will be in error.
To accurately estimate annual root respiration, many individual measurements would have to be made at ambient temperature over the course of the year.
The degree to which root respiration acclimates to climate
warming could affect the global C balance which, in turn,
could affect the extent of climate change. Recent evidence
suggests that ecosystem respiration, not photosynthesis, may
be the main determinant of net ecosystem C exchange in many
forests (Valentini et al. 2000), and the degree to which respiration rates increase as temperatures increase will determine the
sink strength of terrestrial ecosystems (Grace and Rayment
2000). If respiration rates increase rapidly as temperatures increase (i.e., no acclimation), a positive feedback could occur,
causing atmospheric CO2 concentration, and subsequently
global temperatures, to increase more rapidly (Woodwell and
Mackenzie 1995). If acclimation of the components of soil
respiration occurs, this feedback loop will be weakened (Luo
et al. 2001), reducing the potential temperature increase. Cox
et al. (2000) recently predicted mean global warming of 5.5 °C
by 2100 when feedback between the C cycle and climatic
warming was included, compared with a 4 °C increase without
the feedback. Increases for mean land temperature were even
more extreme: 8 °C from 1860 to 2100 with the feedback
mechanism, and 5.5 °C without the feedback.
In 1998 and 1999, we measured root respiration in the field
at ambient soil temperature throughout the snow-free season
in a northern hardwood forest dominated by sugar maple (Acer
saccharum Marsh.) and in a red pine (Pinus resinosa Ait.)
plantation in Michigan. Objectives of the research included:
(1) determining the effects of temporal variations in soil temperature and soil matric potential on specific respiration rates
for the two forest types; and (2) testing for evidence of temperature acclimation in response to seasonal changes in soil temperature by comparing field respiration rates measured at
ambient soil temperature over time to previous respiration
measurements made in the laboratory using a temperature series on a single date. A further test for acclimation of sugar maple root respiration utilized previous and new data for
respiration rates determined in the laboratory at constant reference temperatures of 6, 18 and 24 °C. These measurements
were made at various times during the year when field soil
temperatures varied from 0.4 to 16.8 °C. Lower respiration
rates at a reference temperature during periods of high soil
temperatures would indicate the existence of partial acclimation. Each of the study sites had both control and N-amended
study plots, so the effects of long-term N additions on root respiration rates were also assessed.
NO TEMPERATURE ACCLIMATION FOR ROOT RESPIRATION
(Bouma et al. 1997a, 1997b, Bryla et al. 2001, Burton and
Pregitzer 2002). We tested a subset of our field root samples
for a possible [CO2] effect by determining respiration rates at
both 350 and 1000 µl l –1, and found no effect of [CO2] on root
respiration rates of either sugar maple or red pine measured in
the field (Burton and Pregitzer 2002).
Laboratory root respiration at constant reference
temperatures
In previous work, we measured root respiration of sugar maple
trees in the laboratory at fixed temperatures of 6, 18 and 24 °C
(Site A in Burton et al. 1996, Burton et al. 1998). The measurements were made at various times of the year during 1994,
1995 and 1996, with ambient soil temperatures during the preceding 4 days ranging from 6.1 to 16.8 °C. These data and data
from two additional sampling dates in 1997 (ambient soil temperatures of 0.4 and 14.3 °C) were examined for evidence of
temperature acclimation. The site did not experience dry soil
conditions during any of these sampling dates (Burton et al.
1998).
Roots for these experiments were obtained from 10-cm
deep by 5.4-cm diameter soil cores collected from four random locations per plot and transported in coolers to the laboratory for processing (less than 30 min travel time per site). In
the laboratory, the four cores per plot were combined. Fine (≤
1.0 mm), non-woody, live roots were then sorted by hand from
the composite sample and rinsed free of soil and organic matter with deionized water. Respiration of 0.5 g (fresh mass) subsamples was measured as Ο2 consumption with gas-phase O2
electrodes (Model LD 2/2, Hansatech Instruments, Norfolk,
U.K.) connected to constant temperature circulating water
baths (Burton et al. 1996, Zogg et al. 1996). Root samples
were allowed to equilibrate to the measurement temperature
for 20 min, before O2 consumption was monitored for 40 to
60 min. During this period, O2 consumption rates declined
only slightly (less than 5%). Three complete O2 electrode systems were run simultaneously, allowing respiration measurements to be performed on separate root samples at 6, 18 and
24 °C within 3 h of sample collection. A complete instantaneous temperature series was performed for all six plots on
each of the 10 measurement dates. A similar temperature series was determined for the red pine plantation on a single
measurement date in 1997 (Burton et al. 2002).
Statistical analyses
The effect of N additions on root respiration rates measured in
the field was analyzed by repeated measures analysis of variance. Separate analyses were used for the sugar maple and red
pine sites, because the N additions differed in form, duration
and rate of application. Linear regression was used to model
the effects of temperature, soil matric potential and fine root N
concentration on specific root respiration rates measured in
the field at each site, with the natural log of respiration as the
response variable. Regression models were estimated based
on data for all individual samples from a site. The temperature
slope coefficient for each forest type was then used to calculate its respiratory Q10 (Q10 = e10(T slope)). Differences between
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sisted of five to seven excised root mats, each comprising an
intact network of root segments containing primarily first-,
second- and third-order roots (see Pregitzer et al. 1998 for an
illustration of a typical root mat). During excision, roots were
damaged only at the locations where the intact root networks
were detached (i.e., five to seven locations per sample). Detailed examinations of similar root mats suggest that first-order roots contributed about 50% of the root length sampled
and second-order roots contributed about 25% (Pregitzer et al.
2002). Typically, one sample was analyzed from each plot at a
site on each measurement date. In the two cases where two
samples from a plot were analyzed on a given date, mean values for the two samples were used in subsequent repeated
measures analysis of variance.
Total root collection time was about 15 min, and samples
(about 2–4 g fresh weight) were immediately placed in a respiration cuvette attached to an infrared gas analyzer (IRGA,
CIRAS-I portable gas analyzer, PP Systems, Haverhill, MA).
The IRGA and cuvette were configured in an open system,
with root respiration rate determined as the difference between
the amounts of CO2 entering and leaving the cuvette. Steady
respiration rates were achieved within 15 to 20 min after placing a sample in the cuvette. The input CO2 concentration
([CO2]) for the cuvette was maintained at 1000 µl l –1 to approximate soil [CO2]. This value is slightly lower than the
[CO2] typically found near the soil surface where our root
samples were taken (1200 µl l –1, Burton et al. 1997; 1350 µl
l –1, Yavitt et al. 1995; and 1023 µl l –1, Fernandez et al. 1993).
The one-piece base of the aluminum root respiration cuvette
was 5 cm in diameter, with an internal chamber for roots that
was 5 cm in depth with a volume of 76 cm3. Beneath the respiration chamber was a solid aluminum plug 12 cm in length.
The entire 17-cm-long aluminum base was inserted into the
soil, with only the upper 1 cm of the base and the cuvette top
above the soil surface. This allowed roots inside the cuvette to
be maintained at ambient soil temperature during measurement (verified by comparing temperatures measured by a
thermistor inside the cuvette, in contact with the root sample,
to soil temperatures adjacent to the cuvette).
Following respiration measurements, root samples were
placed on ice in coolers until they could be returned to the laboratory (less than 3 h). In the laboratory, root samples were
frozen until a later date when they were cleaned of any adhering soil and organic debris (≤ 5% of sample mass), dried, and
analyzed for N with an elemental analyzer (Carlo Erba NA
1500 NC, CE Elantech, Lakewood, NJ). Microbial respiration
in the adhering soil and organic debris would have been measured as root respiration, but rates of microbial respiration per
gram of forest soil material (Zak et al. 1999) are often orders of
magnitude less than those we measured per gram of root tissue. Thus the contribution of these materials to measured root
respiration rates should be less than 5% of the reported values.
The [CO2] at which measurements are made can potentially
affect root respiration rates of tree species (Qi et al. 1994, Burton et al. 1997), with higher measurement [CO2] resulting in
lower respiration rates. However, recent reports suggest that
this CO2 effect does not exist for roots of many species
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BURTON AND PREGITZER
Q10 values calculated from field respiration measurements
made across the growing season (long-term Q10) and those calculated for instantaneous laboratory temperature series (shortterm Q10) were assessed by comparing regression slope coefficients for temperature by the Student’s t-test in a fashion analogous to that for testing differences between population means
(Zar 1984). Regressions of respiration rate versus ambient soil
temperature during the previous 4 days were used to examine
respiration rates measured in the laboratory at constant temperatures of 6, 18 and 24 °C for evidence of seasonal acclimation of root respiration.
For both forest types, root respiration rates in the field followed changes in soil temperature when soils were moist and
were reduced when soils were dry (Figure 1). Because root
respiration was unaffected by N additions at either site (Table 1), data from all samples were used to develop single regression relationships for each site. Fine root respiration rates
for sugar maple were best predicted by the relationship:
ln(R ) = – 0.41 + 0.052 N + 0.55M + 0.086T
(r 2 = 0.77, P < 0.0001, N = 104)
where R is specific root respiration (nmol CO2 g –1 s –1), N is tissue N concentration (g kg –1), M is soil matric potential (MPa),
and T is temperature (°C). Soil temperature and soil matric potential explained most of the variation among sample dates,
whereas tissue N concentration primarily explained variation
among individual samples within sampling dates. This effect
was not a result of the N additions, because root N concentration varied more within treatments than between treatments
and was not significantly affected by N additions (P = 0.11 for
repeated measures analysis of variance).
For the red pine site, specific respiration rates in field samples were predicted by the relationship:
ln(R ) = – 013
. + 0.67M + 0109
. T
(r 2 = 0.76, P < 0.0001, N = 54 )
The long-term Q10 values calculated from the slope coefficients for temperature were 2.4 for sugar maple and 3.0 for red
pine. Ignoring root N concentration at the sugar maple site decreased the predictive ability of the relationship by about 6%,
but did not affect the calculated long-term Q10 value. Ignoring
soil matric potential reduced the amount of variation accounted for at both sites by about 8% and caused the long-term
Q10 values to decline to 2.2 and 2.4 for sugar maple and red
pine, respectively.
Laboratory measurements of root respiration made at different times of the year indicated no relationship between mean
ambient soil temperature during the 4 days before sampling
and root respiration rates at reference temperatures of 6 and
18 °C (Figure 2), and indicated only a very weak relationship
between ambient soil temperature and root respiration at 24 °C
Figure 1. Root respiration rates under moist, moderate and dry soil
conditions for the sugar maple and red pine sites. The regression lines
indicate the temperature response for each species when soil matric
potential was high (–0.067 MPa for sugar maple and –0.086 MPa for
red pine). For sugar maple, the regression line was calculated based
on the site mean N concentration of 17.5 g kg –1. Scatter of the moist
data points around the regression line for sugar maple is largely a result of variation in N concentration among individual samples.
(P = 0.08, slope = –0.09). Short-term Q10 values were calculated for each of the 10 sample dates portrayed in Figure 2.
These short-term Q10 values averaged 2.7, and they were unrelated to mean soil temperature during the preceding days (P =
0.22). The 4-day period for soil temperature was chosen based
on the number of days needed for acclimation to occur in laboratory studies in which acclimation of root respiration has
been observed (Bryla et al. 1997, 2001, Gunn and Farrar
1999). The use of shorter time periods or same-day soil temperatures did not alter the results.
Discussion
Acclimation of respiration to high temperatures can result in
either a lower slope (Q10) for the temperature-response curve
of acclimated tissue or a reduction in the intercept (Atkin et al.
2000a). In either case, the effect of acclimation in laboratory
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Results
NO TEMPERATURE ACCLIMATION FOR ROOT RESPIRATION
Table 1. Repeated measures analysis of variance of the effects of N
additions (30 kg N ha –1 year –1 as NaNO3 for sugar maple and 100 kg
N ha –1 year –1 as NH4NO3 for red pine) on root respiration rates measured in the field at ambient soil temperature during 1998 and 1999.
Source
Sugar maple forest
Between subjects
N addition
Error
Red pine plantation
Between subjects
N addition
Error
Within subjects
Measurement date
Date × N addition
Error
df
MS
F ratio P > F
2.07
4.20
1
4
2.07
1.05
1.97
0.233
376.52
35.30
96.54
16
16
64
23.53
2.21
1.51
15.60
1.46
< 0.000
0.155
0.02
4.12
1
4
0.02
1.03
0.02
0.888
160.09
2.80
21.69
8
8
32
20.01
0.35
0.68
29.52
0.52
< 0.000
0.835
studies is a long-term Q10 (determined by measuring respiration at growth temperatures for plants grown at different fixed
temperatures) that is lower than the short-term Q10 (derived
from instantaneous temperature series conducted on individual plants). For example, Tjoelker et al. (1999a) found that foliar respiration of five tree species grown under controlled
conditions acclimated to elevated temperatures, resulting in
long-term Q10 values for foliar respiration that ranged from 1.1
Figure 2. Relationship between sugar maple root respiration as O2
consumption, at reference temperatures of 6, 18 and 24 °C, and mean
ambient soil temperature (15 cm) during the previous 4 days. Relationships were not significant at any temperature (P values were 0.37,
0.86 and 0.08 for 6, 18 and 24 °C, respectively). Each symbol represents a mean value for samples from six plots. Soil matric potential
did not significantly affect the results, because dry conditions did not
occur at the site for any of the sample dates involved (Site A in Burton
et al. 1998).
to 1.9 compared with short-term Q10 values, determined for
the same plants, of 2.1 to 2.4. Similarly, if plant tissues acclimate quickly to seasonal changes in temperature in the field,
the net result should also be a long-term Q10 (determined from
measurements made at ambient temperature throughout the
growing season) that is lower than the short-term Q10 value
(determined using temperature series at individual points in
time). In the extreme case of rapid, full acclimation (homeostasis), respiration rates measured in the field at ambient temperature would produce a long-term Q10 of 1.0.
For the sugar maple and red pine study sites, we periodically
measured respiration rates in the laboratory across a temperature series from 6 to 24 °C. Short-term Q10 values determined
from these measurements were 2.6 (Burton et al. 1996) to 2.7
(based on all data summarized in Figure 2) for the sugar maple
forest and 3.0 for the red pine plantation (Burton et al. 2002).
The long-term Q10 values determined in this study (based on
respiration rates measured at ambient temperature over the
growing season) were slightly, but not significantly lower for
the sugar maple forest (2.4) and unchanged for the red pine
plantation (3.0). The long-term Q10 for sugar maple would
need to be 0.7 units lower than the short-term Q10 to be significantly different at the 0.05 level of probability.
Measurements over time at a constant reference temperature are considered to be a reliable test for the occurrence of
partial acclimation in response to either seasonal changes in
temperature or to warming treatments (Atkin et al. 2000a). For
sugar maple, our respiration measurements from 1994 to 1997
at reference temperatures of 6 and 18 °C showed no evidence
of temperature acclimation in response to seasonal changes in
soil temperature, and measurements at 24 °C showed only
marginal evidence of acclimation (Figure 2). Even if the 24 °C
reference data were the result of real acclimation, they would
indicate only partial acclimation. For example, the increase in
root respiration as temperatures increased by 12 °C would be
10% less due to this partial acclimation. This is much less than
the 40% average reduction in respiration attributable to acclimation reported by Tjoelker et al. (1999a) for five tree species
grown in the laboratory at temperatures that differed by 12 °C.
For red pine, the short-term Q10 was based on laboratory
data from only one date; thus we cannot make a comparison
similar to that illustrated in Figure 2 for sugar maple. However, the maximum long-term Q10 based on the field data (3.0),
relative to the published range of short-term Q10 values for
root respiration (1.1–3.1; Atkin et al. 2000a, Burton et al.
2002), is fairly strong evidence that little, if any, intra-annual
temperature acclimation of root respiration occurred in the
field in response to seasonal changes in soil temperature.
For root respiration, evidence of seasonal acclimation to
shifts in ambient soil temperature has been found for grassland
species (Fitter et al. 1998), but not for roots of woody
perennials. Fairly rapid temperature acclimation of root respiration has been seen in tree seedlings grown at one constant
temperature and then shifted to another constant temperature
(Bryla et al. 1997, 2001) and in 9-year-old grapefruit (Citrus
paradisi Macf.) trees in which soil was heated to approximately 10 °C above ambient but allowed to fluctuate naturally
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Within subjects
Measurement date
Date × N addition
Error
SS
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BURTON AND PREGITZER
Figure 3. Soil temperature profiles during early, mid- and late growing season periods at the sugar maple and red pine sites in 1999.
leaves and roots to efficiently match their activity to the availability of growth-limiting resources. In temperature-step
laboratory experiments that have shown acclimation, availability of N and other nutrients was typically not increased
with temperature (Bryla et al. 1997, Tjoelker et al. 1999a) as
might be expected to occur under field conditions.
It is possible that roots of some temperate tree species
would not acclimate to seasonal changes in soil temperature,
but would acclimate to increases in annual temperatures associated with global warming. If annual temperatures increased,
but total annual nutrient requirement did not, then root metabolic uptake potential would exceed demand on an annual basis. In this case, downward adjustment of annual root system
metabolic activity might be beneficial. This could occur
through the construction of roots with lower protein nitrogen
and amino acid concentrations. Such roots would presumably
have a low respiration rate, in agreement with the many reports of strong correlations between root tissue N and respiration rate (Burton et al. 1996, 2002, Ryan et al. 1996, Zogg et al.
1996). Essentially, these tree roots would contain less metabolic machinery that would function at a higher rate because of
elevated temperatures and could therefore accomplish similar
amounts of work as roots with higher N concentrations in a
cooler environment. If such a longer-term change occurred in
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(Bryla et al. 2001). In this latter study, however, acclimation
occurred only above 23 °C.
A variety of factors may have contributed to the failure of
root respiration to acclimate to seasonal changes in soil temperature in our study. In experiments that held elevated temperatures constant, acclimation of root respiration took 4 to
5 days to occur (Bryla et al. 1997, 2001, Gunn and Farrar
1999). Time spans of several days for acclimation have also
been reported for temperature-step experiments examining foliar dark respiration (Atkin et al. 2000b). Natural fluctuations
in soil temperatures in the field may reduce the degree of acclimation that can occur. Roots within 5 cm of the soil surface at
both of our sites experienced temperature shifts of 5 to 10 °C
over time spans of one to several days throughout the growing
season (Figure 3), which may have prevented discernible acclimation from occurring. There may also be a temperature
threshold below which acclimation of root respiration does not
occur. Bryla et al. (2001) did not find temperature acclimation
of citrus root respiration below a temperature of 23 °C, and
soil temperatures at 5-cm depth in the heated treatment in
which they found acclimation were often in the 32 to 37 °C
range. Soil temperatures at the 5-cm depth for our sites
reached maxima of 19.9 °C at the sugar maple site and 22.0 °C
at the red pine plantation. Adjacent to the soil surface, temperatures were occasionally higher, but never for longer than 10 h
during the day, after which they decreased considerably overnight (1-cm depth in Figure 3). Finally, root respiration of
some species simply may not acclimate to temperature. For
example, there have been reports of no temperature acclimation in root respiration for Picea engelmannii, Abies lasiocarpa and Picea glauca (Sowell and Spomer 1986, Weger and
Guy 1991). Larigauderie and Körner (1995) studied foliar respiration of 19 species and found a range from full to no temperature acclimation. Gunderson et al. (2000) reported only a
small (10%) temperature acclimation for foliar dark respiration of sugar maple saplings grown at temperatures 4 °C above
ambient.
It is likely beneficial for acclimation of foliar dark respiration to occur. The same may not be true for root respiration, at
least relative to seasonal changes in soil temperature. Availability of resources for photosynthesis (light, CO2) at the leaf
surface would not be greatly changed by a warm period in the
middle of the growing season. However, the supply rate of nutrients to roots could be significantly increased by an increase
in soil temperature through effects on mineralization of organic nutrients (MacDonald et al. 1995, Zak et al. 1999) and
ion diffusion. Down-regulation of foliar dark respiration during such a warm period might limit C losses without greatly
affecting the rate of photosynthesis. In roots, high metabolic
activity (respiration rates) during warm, moist conditions
would allow for rapid nutrient uptake and assimilation during
the co-occurring periods of enhanced nutrient supply (Pregitzer et al. 2000). Temperature acclimation during such times
and the accompanying reduction in metabolic activity could
reduce nutrient uptake. Acclimation to seasonal changes in
temperature in foliage, but not in roots, might allow both
NO TEMPERATURE ACCLIMATION FOR ROOT RESPIRATION
Conclusions
Specific root respiration rates in sugar maple and red pine forests in Michigan were highly correlated with both soil temperature and soil water availability. Long-term Q10 values (based
on field measurements of root respiration) were similar to
short-term Q10 values (based on instantaneous temperature series in the laboratory) for both species, and sugar maple root
respiration at constant reference temperatures did not vary significantly as ambient soil temperature changed. This suggests
that root respiration in these species undergoes little, if any,
acclimation to seasonal changes in soil temperature. For both
sugar maple and red pine, results from laboratory temperature
series performed at a single point in time appeared to be applicable to field conditions throughout the year, although a series
of field measurements spaced over the growing season would
be preferable. Our results for two growing seasons do not preclude possible adjustment of root system activity to the sustained increases in mean annual temperature predicted in
global climate change scenarios. Such adjustment could cause
large increases in ecosystem C losses from root respiration unless there are reductions in either root biomass or root metabolic capacity.
Acknowledgments
The authors thank Kate Bradley, Angela Bartnik and Sarah Riter for
their assistance in the field and laboratory. This research was supported in part by the U.S. National Science Foundation (grants DEB
0075397, DEB 9615509, DBI 9413407).
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