Directory UMM :Data Elmu:jurnal:T:Tree Physiology:vol17.1997:

Tree Physiology 17, 179--185
© 1997 Heron Publishing----Victoria, Canada

Root carbohydrate reserves, mineral nutrient concentrations and
biomass in a healthy and a declining sugar maple (Acer saccharum)
stand
XUAN LIU1,2 and MELVIN T. TYREE1,3
1

Department of Botany, University of Vermont, Burlington, VT 05405--008, USA

2

Present address: Department of Botany and Plant Sciences, University of California, Riverside, CA 92521--0124, USA

3

Present address: USDA Forest Service, Northeastern Forest Experiment Station, P.O. Box 968, Burlington, VT 05402, USA

Received April 3, 1995

Summary Soil and root characteristics were contrasted between a ‘‘declining’’ and a ‘‘healthy’’ sugar maple (Acer saccharum Marsh.) stand in Vermont, USA. The declining stand
had lower basal area increment and more crown dieback than
the healthy stand. Soil pH and base cation content were lower
and soil water content was higher at the site of the declining
stand than at the site of the healthy stand, whereas soil temperature did not differ significantly between the sites.
In live fine roots, concentrations of K and Ca were marginally (P < 0.07) lower in the declining than in the healthy stand,
whereas concentrations of N, P, Mg, and Al were not significantly different (P = 0.13 to 0.87) between stands. Starch and
soluble sugar concentrations of fine and coarse roots did not
differ significantly between stands, indicating that crown dieback did not affect carbohydrate supply to the roots in the
declining stand. Throughout the growing season, the standing
live and dead root biomass were significantly higher in the
declining stand than in the healthy stand, indicating that more
carbon was allocated to roots and that root turnover was higher
in the declining stand than in the healthy stand.
Keywords: forest decline, forest health, nutrition.

Introduction
Extensive sugar maple (Acer saccharum Marsh.) decline has
been reported in northeastern Canada and the USA. Foliar
discoloration, crown dieback and reduced basal area growth

are characteristic symptoms of sugar maple decline (Bernier
et al. 1989, Allen et al. 1992, Kolb and McCormick 1993,
Wilmot et al. 1995). The soil in declining stands is often low
in nutrient content, and this is reflected in low foliar Mg or Ca
concentrations, or both, and in low photosynthetic rates of
branches exhibiting dieback (Ellsworth and Liu 1994, Wilmot
et al. 1995, Liu et al. 1997). However, although acidic soil with
low base cation availability has been implicated in sugar maple
decline (Wilmot et al. 1995), few studies have focused on the
physiological status of roots during decline (Adams and
Hutchinson 1992). We postulated that the root systems of sugar

maple trees may be altered or exhibit abnormalities in acidic
soil with low base cation availability.
To test this assumption, we evaluated alterations in root
system dynamics in the context of sugar maple decline. Specifically, we compared root mineral nutrient status, carbohydrate reserve status, and root biomass distribution during the
growing season in a declining and a healthy stand of sugar
maple in Vermont.

Materials and methods

Study sites
A declining and a visibly healthy sugar maple stand growing
in similar soils were selected in Vermont (Wilmot et al. 1995).
The healthy stand was located at Fairfield (44°48′ N, 72°59′ W,
elevation 165 m, slope 15%), and the declining stand was
located approximately 40 km away at Proctor Maple Research
Center, Underhill Center (PMRC, 44°31′ N, 72°53′ W, elevation 440 m, slope 10%). The criteria for characterizing the
stands included percentage crown dieback, foliar chlorosis,
and reduction in annual basal area growth.
Details of the stands have been presented by Liu et al. (1997)
and Wilmot et al. (1995). Briefly, the soil at the site of the
declining stand is a Marlow coarse loam (coarse-textured
Haplorthod) with a pH of 3.7 ± 0.1, whereas the soil at the site
of the healthy stand is a Stowe silt loam (fine-textured Haplorthod) with a pH of 4.9 ± 0.1. At both sites, the O and A horizons
were about 5 cm and 10 cm thick, respectively, and the A plus
B horizons were about 50 cm thick, under which the parent
material was glacial till (Wilmot et al. 1995). Soil Ca and Mg
concentrations were 1547 ± 277 and 162 ± 44.9 mg g −1,
respectively, at the site of the healthy stand, and the corresponding values at the site of the declining stand were 1138 ±
88 and 96.5 ± 5.3 mg g −1 (Wilmot et al. 1995). Total sulfur

deposition rates were 8.3 and 6.6 kg ha −1 year −1 at the declining and healthy sites, respectively. Total nitrogen deposition
rates were 6.0 and 4.9 kg ha −1 year −1 at the declining and
healthy sites, respectively. The dominant sugar maples were

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LIU AND TYREE

greater than 200 years old and 125--145 years old in the healthy
and declining stands, respectively. Stand basal areas (summed
tree basal area for all trees per unit ground area (Spurr and
Barnes 1980) were 27.6 ± 4.7 and 34.2 ± 5.4 (cm2 m −2) for the
healthy and declining stands, respectively. Other tree species
present were American beech (Fagus grandifolia J.F. Ehrh.),
yellow birch (Betula alleghaniensis Britt.), American ash
(Fraxinus americana L.) and striped maple (Acer pensylvanicum L.). Their total basal area accounted for less than 9% of
the stand basal area of each stand.
Root sampling
Sequential core sampling (Persson 1978, 1980, Grier et al.
1981, Vogt and Persson 1991) was used to estimate root

biomass. Samplings were made in late April (just before bud
flush), late May (during flushing), early August (after the
crowns were fully developed) and late October 1992 (onset of
dormancy). Four adjacent 16 × 16 m2 plots in each stand were
established for coring. The steel soil corer was 0.9-m long and
50.8-mm in diameter. At each sampling time, four soil cores
were taken randomly from each plot with the restriction that
sampling be at least 1 m away from any big tree to avoid
possible variation in coarse root biomass (Persson 1980). Soil
cores were extracted sectionally at depths of 0--5 cm, 5--10
cm, 10--30 cm, 30--40 cm, and 40--50 cm. It took two days to
process all of the soil cores from the two stands at each time.
Each soil core section was sealed in a plastic bag and stored at
1 °C until processed. The storage periods were less than 4
months and analyses were done randomly so as not to bias
cores from the two sites by storage time.
Root processing
Soil was removed from roots by washing through 500 µm
sieves (Böhm 1979, Vogt and Persson 1991). Roots were kept
moist, sorted into fine roots (diameter ≤ 2 mm) and coarse roots

(diameter > 2 mm) and then separated into three categories:
sugar maple roots, other tree roots, and roots of fern and other
non-tree species. The roots of sugar maple and other tree
species were further sorted into dead and live classes with the
aid of a dissecting microscope and forceps.
The roots from both stands rarely showed signs of disease,
but some fine roots were infected with mycorrhizae. Sugar
maple roots were morphologically distinguishable from roots
of other tree species (Goldfarb et al. 1990, Bauce and Allen
1992). Typically, sugar maple fine roots were cream to medium
brown in color, and had short and beaded-looking rod or round
root tips, some beaded long fragments and quite uniform
thickness among different branching orders. Sugar maple
coarse roots had rough furrowed bark of a cream to barely
brown-red color with widely spaced wavy-lines on the bark.
Roots of other tree species were mostly of beech, birch and
cherry. The distinctive differences between the fine roots of
these species and those of sugar maple included very short, less
branching root tips, much smaller lateral branches than main
branches, uneven thickness among different branching series

and darker red color. Coarse roots of beech, birch and cherry
typically had bark with black lines on raised ridges; the black

lines frequently crossed over each other. Roots of other tree
species such as ash and striped maple were rare and were easily
separated from sugar maple roots because they were whitish in
color. The major non-tree species was fern and its roots were
distinctive, having a smooth surface and a fleshy appearance.
Dead and live fine roots were distinguished by their color,
resiliency, turgidity and adhesion between the stele and cortex
or periderm. Typically, dead roots were wrinkled, brittle and
easily fragmented and had discolored phloem. In cross section,
the stele was dark brown or black and the periderm was
detached from the stele.
After washing and sorting, roots were transferred to vials,
dried in an oven at 70 °C for 48 h and weighed to ± 0.1 mg.
In addition to the major integral root networks, other detached fine root segments mixed with forest litter in the soil
were retained in the sieve. These segments were mostly dead
sugar maple roots. In soil sections from 0 to 40 cm below the
soil surface, these dead fine root segments were comprised

mainly of root tips and were difficult to isolate from the other
forest litter. Therefore, only a quarter of the mixture retained
in the sieve was analyzed. The amount of roots in the quarter
subsample was used to estimate the amount of roots in the
whole retained sample. Ignoring this part may account for up
to a 50% error in the estimation of root biomass (Grier et al.
1981).
Soil temperature
Soil temperatures at depths of 0 cm and 15 cm from the surface
of the mineral soil were monitored between 1130 and 1530 h
in late May, early July, early August and mid-October of 1992.
Two constantan wires connected with plugs were buried close
to each other at the two depths in each stand, and temperatures
were determined simultaneously in the two stands to an accuracy of 0.1 °C.
Soil water content
Soil water content from the soil surface to a depth of 30 cm was
determined concurrently with soil temperature. Three soil
cores were randomly taken from each of the four plots in each
stand with a 20-mm diameter soil auger and immediately put
in preweighed metal boxes. Each metal box with soil sample

was weighed and dried in an oven at 105--107 °C for 48 h.
Gravimetric soil water content on a dry weight basis was then
calculated.
Root non-structural carbohydrate
Sugar maple roots were isolated from soil cores within 4 days
after sampling, then immediately dried at 70 °C for 48 h in an
oven. After being weighed, the samples were ground to pass a
40-mesh metal screen. Bark was removed from the coarse
roots. For each root biomass assay, about 0.15 g of dry ground
roots from the core section between 0 and 30 cm was used. Two
assays were made for each root class of each core, and three
cores were used for each stand. Root glucose concentration
was assayed by the INT enzymatic method. Root starch was
converted to glucose with amyloglucosidase (Fluka 10115,
Fluka Chemical Corp., St. Louis, MO); sucrose was converted

ROOT CARBOHYDRATE, NUTRITION AND BIOMASS

to glucose with invertase, (Sigma I-4504, Sigma Chemical, St.
Louis, MO); and fructose was converted to glucose with phosphoglucose isomerase, and then analyzed separately by the

same INT enzymatic method (Hendrix 1993).
Root mineral nutrients
Dry live fine roots from the soil core section between 0 and
10 cm were ground to pass through a 40-mesh metal screen
and their mineral nutrients were assayed by the Agriculture
Testing Laboratory, University of Vermont. The ground roots
were digested with a mixture of concentrated HClO4 and HNO3
and P, K, Ca, Mg, Al were measured with an inductively
coupled plasma atomic emission spectrometer (Plasmaspec.
2.5, Leeman Labs, Lowell, MA). Root total nitrogen was
assayed by the Dumas method with a CHN element analyzer
(Leeman Labs).

181

Table 1. Soil temperature (°C) in the healthy and declining stands
(n = 4 for each stand) measured before 1530 h on four sampling dates
in 1992. Soil depth was measured from the mineral soil surface. Values
are means ± 1 SE.
Date

Depth
(cm)

Healthy

Declining

t-test
P-value

Late May

0
15
0
15
0
15
0
15

11.6 ± 0.4
9.7 ± 0.2
15.0 ± 0.4
13.5 ± 0.4
16.4 ± 0.5
14.2 ± 0.2
9.0 ± 0.2
9.5 ± 0.3

10.8 ± 0.5
10.1 ± 0.4
14.4 ± 0.4
12.6 ± 0.2
16.8 ± 0.3
14.5 ± 0.1
8.7 ± 0.2
9.6 ± 0.2

0.654
0.402
0.543
0.267
0.183
0.070
0.169
0.803

Early July
Early August
Mid-October

Statistical analysis
Differences between measured soil and root characteristics of
the stands were tested by t-test at P ≤ 0.05 significance level.
Seasonal changes in root biomass, carbohydrate concentrations and differences in root biomass density between different
soil depths were analyzed by the multiple-comparison (Bonferroni) method at P < 0.05 significant level. Covariance analysis was used to assess the effect of stand basal area on root
biomass; the stand was considered as the nominal variable and
stand basal area as the covariable. The corresponding
LSMEAN t-test was made to correct the means affected significantly by basal area. All analyses were done with SAS
software (SAS Institute, Cary, NC).

Results and discussion
Soil temperature and water content
Edaphic factors, especially mineral nutrient status, pH, temperature and water, define the environment for the root and
hence its physiological status, which in turn, directly affects
shoot physiology (Caldwell et al. 1989, Schneider et al. 1989).
Both soil temperature and soil water content in the declining
stand were favorable for root processes. From May to October,
soil temperatures at 0 cm and 15 cm from the mineral soil
surface in the two stands were similar (Table 1). Soil at the site
of the declining stand had a significantly higher water content
than soil at the site of the healthy stand from late April to late
October (Figure 1). No difference in leaf water stress was
found between the two stands in a related study (Liu et al.
1997), indicating that water stress did not play a role in decline.
Edaphic factors that were less favorable for root processes in
the declining stand than in the healthy stand included a lower
base cation status and a lower soil pH (Wilmot et al. 1995).
Mineral nutrition of roots
Live fine roots of trees in both stands had similar concentrations of N, P and Mg (Table 2). But fine roots in the declining
stand had marginally lower K and Ca concentrations than fine
roots in the healthy stand (Table 2).

Figure 1. Seasonal course of gravimetric soil water content (%, means
± 1 SE, based on dry weight) at the sites of the healthy and declining
stands. Twelve soil cores were taken on each date for each stand.
Significant differences between the two stands are indicated by asterisks: ** = P ≤ 0.01, no asterisk = P > 0.05.

Table 2. Mean (± SE) macronutrient concentrations (µg gdw−1), Al
concentrations (µg gdw−1) and the ratio of Ca/Al (mean ± SE) of live
fine roots (diameter ≤ 2 mm) from 0--10 cm deep soil collected in early
August 1992 from healthy (Fairfield) and declining (PMRC) sugar
maple stands (n = 6 for each stand). Significance level on t-test for the
differences between the two stands is P ≤ 0.05.
Element

Healthy

Declining

P-value

N
P
K
Ca
Mg
Al
Ca/Al

11200 ± 300
580 ± 70
720 ± 120
5600 ± 1,100
720 ± 110
3100 ± 400
2.11 ± 0.65

11000 ± 400
630 ± 20
400 ± 60
3100 ± 200
570 ± 60
4000 ± 300
0.79 ± 0.06

0.873
0.494
0.060
0.065
0.245
0.126
0.083

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LIU AND TYREE

Low soil pH may be the common factor explaining the
results in Table 2 and in other studies (Tattar 1978, Meyer et al.
1988, Oren et al. 1988b, Schneider et al. 1989). The lower soil
pH in the declining stand than in the healthy stand (3.7 versus
4.9) might inhibit K and Ca uptake (Table 2) (cf. Schneider
et al. 1989). Several other studies have shown that Ca concentration is low in fine roots growing in acidic soils with low
soluble Ca concentration (Oren et al. 1988b, Schneider et al.
1989, Adams and Hutchinson 1992).
Base cation leaching and increased accumulation of soluble
Al3+, which are caused by soil acidification (Ulrich et al. 1980),
have been linked to many cases of forest decline (Schneider
et al. 1989, Adams and Eagar 1992, McLaughlin and Kohut
1992). High concentrations of mobile Al3+ in the soil could
inhibit Ca uptake, and cause increased accumulation of Al3+
in plants (Ulrich et al.1980, McLaughlin 1985, Marschner
1986, Shortle et al. 1988). However, we found no significant
difference in Ca/Al ratios of fine roots between the two stands,
although Ca/Al was less than one in the declining stand and
greater than one in the healthy stand (Table 2).
Major non-structural carbohydrate reserves in roots
Generally, fine and coarse root sugar (sucrose + fructose +
glucose) and starch concentrations were similar in the two
stands throughout the growing season (Figures 2A and 2B).
Before and during bud flush in spring, root starch concentrations tended to be lower in the declining stand than in the

Figure 2. Seasonal changes in concentrations of starch and soluble
sugars (sucrose + fructose + glucose) (means ± 1 SE, based on dry
weight) in live fine roots (A) and live coarse roots (B) of sugar maple
trees in the healthy and declining stands. Three soil cores were measured on each date for each stand. Significant differences between the
two stands are indicated by an asterisk (0.01 < P < 0.05).

healthy stand, but only in late April was a marginally significant difference found (Figure 2A).
Although the declining trees were partly defoliated as a
result of small branch dieback and had a depressed photosynthesis rate in the remaining nutrient-poor foliage (Liu et al.
1997), they did not show a reduction in stored carbohydrates
in roots < 1 cm diameter (Figure 2). This finding is consistent
with other maple studies (Oren et al. 1988a, Renauld and
Mauffette 1991), and indicates that crown dieback did not
affect carbohydrate supply to the roots in the declining stand.
Root biomass accumulation and distribution
Total root biomass per ground area (Rm/a) was computed from
all roots found between the surface and a soil depth of 40 cm.
Covariance analysis showed that there was no significant effect
of stand basal area on Rm/a in sugar maple except in late
October when live fine root biomass was significantly affected
by stand basal area. When the Rm/a values for October for the
two stands were corrected for the effect of stand basal area and
the corrected means were compared, we found that more
carbon was allocated to the roots of declining trees than to the
roots of healthy trees. The Rm/a of fine and coarse roots in the
declining stand was high (Figure 3) compared to the root
biomass reported for other mature conifer and hardwood forests (Persson 1980, Grier et al. 1981, McClaugherty et al.
1982, Nisbet and Mullins 1986, Meyer et al. 1988, Bauce and
Allen 1992). The Rm/a of fine and coarse roots of the other tree
species (mainly beech and birch) was low compared to sugar
maples for both stands because of their low basal area (Figure 4), and was not significantly different between the two
stands.
The distribution of root biomass among soil horizons was
expressed as root density (dry mass per volume of soil = Rm/v).
For each root class, Rm/v was computed as a seasonal mean over
the four sampling times between late April and late October
(Figure 5, 6). The Rm/v of fine roots of sugar maple and other
tree species was significantly different among the different soil
horizons (depths) for both stands (P < 0.05, see Figure 5, 6).
For both sugar maples and other tree species in the healthy
stand, more than 64% of live fine roots were distributed in the
O to A horizons (depth of 0--10 cm) and Rm/v was significantly
higher in the O--A horizon than in the B horizon (soil depth of
> 10 cm), except at a soil depth of 10--30 cm (cf. Figures 5A
and 6A). Less than 8% of live fine roots were distributed in
deep soil (40--50 cm depth), and very few fine roots were
found below 50 cm in either stand for both sugar maples and
other tree species (Figures 5A and 6A). The difference in live
fine Rm/v between the two sugar maple stands was mainly a
reflection of the significantly higher Rm/v at the surface soil
(soil depth of < 10 cm) of the declining stand compared with
the healthy stand (Figure 5A).
The distribution of dead fine roots with soil depth was
similar to that of live fine roots for both sugar maples and other
trees (cf. Figures 5B and 6B), except that the total mass of dead
roots exceeded the total mass of live roots. For sugar maples,
Rm/v of dead fine roots was significantly higher above a soil

ROOT CARBOHYDRATE, NUTRITION AND BIOMASS

183

Figure 3. Seasonal patterns of live (A) and dead (B) fine root (diameter
≤ 2 mm) biomass and live coarse root (diameter > 2 mm) biomass (C)
of sugar maple trees in the healthy and declining stands. Sixteen soil
cores were taken on each date and from each stand. Bars represent
± 1 SE. Significant differences in root biomass between the two stands
are indicated by asterisks: ** = P < 0.01, * = 0.01 < P < 0.05, no
asterisk = P > 0.05.

Figure 4. Seasonal patterns of live (A) and dead (B) fine root (diameter
≤ 2 mm) biomass and live coarse root (diameter > 2 mm) biomass (C)
of tree species other than sugar maple in the healthy and declining
stands. Sixteen soil cores were taken on each date and from each stand.
Bars represent ± 1 SE. No significant differences (P > 0.05) between
the two stands were found.

depth of 30 cm in the declining stand than in the healthy stand
(Figure 5B).
More live coarse roots than fine roots were distributed in the
deeper soil layers, especially for sugar maple (Figures 5 and
6). However, coarse root Rm/v did not differ significantly with
soil depth within a stand.
Our results support the notion proposed by others (SchulteBisbing and Murach 1984, Waring 1987, Adams and Hutchinson 1992) that stand decline or mineral deficiency, or both,
stimulate root production of surviving trees. Reduced stem
growth and increased root biomass accumulation may be inversely related during the course of decline. If net productivity
of the crowns is reduced by dieback of small branches and the
decreased photosynthesis of nutrient-poor leaves (Liu et al.
1997), and if more carbon is invested in fine root growth and
turnover, there will be less carbon available for growth of the
bole in declining trees.
The high live root biomass in the declining stand was associated with a high dead root biomass (Figures 3A and 3B). The

amount of dead root biomass depends on the dynamics of
growth, mortality and decomposition, and stand age (Grier et
al. 1981, McClaugherty et al. 1984, Vogt and Bloomfield
1991). The tentative inference we make from our study is that
there was higher root turnover in the declining stand than in the
healthy stand. The declining stand also had significantly lower
ratios of live/dead roots throughout the growth season than the
healthy stand (data not shown), which is consistent with more
root turnover. The alternative explanations seem less likely,
i.e., that younger stands would naturally have more roots than
older stands or that the declining stand has more roots because
roots live longer and decay more slowly in trees that have poor
stem growth.

Concluding hypothesis
Acidic soil with low base cation availability may be the major
stress underlying sugar maple decline. Wilmot et al. (1995)
demonstrated that shoot dieback was correlated with low soil

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LIU AND TYREE

Figure 5. Distribution of mean root density (kgdw m −3) with soil depth
for live (A) and dead (B) fine roots (diameter ≤ 2 mm) and live coarse
roots (diameter > 2 mm) (C) of sugar maple trees in the healthy and
declining stands. Data are averages from four sampling dates in late
April, late May, early August and late October. Sixteen soil cores were
taken on each date from each stand. Line bars represent 1 SE. Significant differences in root biomass density between the two stands at
different soil depths are indicated by asterisks: ** = P < 0.01, * = 0.01
< P < 0.05, no asterisk = P > 0.05.

Figure 6. Distribution of mean root density (kgdw m −3) with soil depth
for live (A) and dead (B) fine roots (diameter ≤ 2 mm) and live coarse
roots (diameter > 2 mm) (C) of tree species other than sugar maple in
the healthy and declining stands. Data are averages from four sampling
dates in late April, late May, early August and late October, 1992.
Sixteen soil cores were taken for each date and from each stand. Line
bars represent 1 SE. Significant differences in root biomass density
between the two stands in different soil depths are indicated by
asterisks: * = 0.01 < P < 0.05, no asterisk = P > 0.05.

Acknowledgments

pH and low base cation status in the same sugar maple stands
used in this study. Because root biomass was higher in the
declining stand than in the healthy stand, we suggest that shoot
dieback was a consequence of the greater allocation of carbon
to roots, which was likely linked to the nutrient-poor acidic
soil. Despite increased root growth and thus increased root
nutrient uptake capacity, shoots and leaves were nutrient poor.
Low foliar nutrient status has been shown to be correlated with
reduced photosynthesis (Liu et al. 1997), reduced carbon availability and lower shoot growth in the declining stand (Wilmot
et al. 1995).

We thank Philip W. Brett and Greta J. Lowther for their technical
assistance in sampling soil cores, measuring stand basal area and
processing roots from the soil cores. We also extend our thanks to the
Vermont landowner for his generosity in allowing us to use his sugarbush for the study. Research was supported by USDA Special Grant
89-34157-4366 to M. T. T.
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