Summary Soil and root characteristics were contrasted be-tween a ‘‘declining’’ and a ‘‘healthy’’ sugar maple (Acer sac-charum 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 tem-perature did not differ significantly between the sites.
In live fine roots, concentrations of K and Ca were margin-ally (P < 0.07) lower in the declining than in the healthy stand, whereas concentrations of N, P, Mg, and Al were not signifi-cantly 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 die-back 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. Spe-cifically, we compared root mineral nutrient status, carbohy-drate 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, eleva-tion 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 Haplor-thod) 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 corre-sponding 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 declin-ing 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
Root carbohydrate reserves, mineral nutrient concentrations and
biomass in a healthy and a declining sugar maple (
Acer saccharum
)
stand
XUAN LIU
1,2and MELVIN T. TYREE
1,31
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
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 pensylvani-cum 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 de-tached 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 accu-racy 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
to glucose with invertase, (Sigma I-4504, Sigma Chemical, St. Louis, MO); and fructose was converted to glucose with phos-phoglucose 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).
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 concentra-tions and differences in root biomass density between different soil depths were analyzed by the multiple-comparison (Bon-ferroni) method at P < 0.05 significant level. Covariance analy-sis 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 sig-nificantly 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, tem-perature 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 concentra-tions 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).
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 Healthy Declining t-test
(cm) P-value
Late May 0 11.6 ± 0.4 10.8 ± 0.5 0.654 15 9.7 ± 0.2 10.1 ± 0.4 0.402 Early July 0 15.0 ± 0.4 14.4 ± 0.4 0.543 15 13.5 ± 0.4 12.6 ± 0.2 0.267 Early August 0 16.4 ± 0.5 16.8 ± 0.3 0.183 15 14.2 ± 0.2 14.5 ± 0.1 0.070 Mid-October 0 9.0 ± 0.2 8.7 ± 0.2 0.169 15 9.5 ± 0.3 9.6 ± 0.2 0.803
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 aster-isks: ** = 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
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 concen-tration 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 concentra-tions tended to be lower in the declining stand than in the
healthy stand, but only in late April was a marginally signifi-cant difference found (Figure 2A).
Although the declining trees were partly defoliated as a result of small branch dieback and had a depressed photosyn-thesis 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 for-ests (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 (Fig-ure 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
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 (Schulte-Bisbing and Murach 1984, Waring 1987, Adams and Hutchin-son 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 in-versely 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 asso-ciated 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
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
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 avail-ability and lower shoot growth in the declining stand (Wilmot et al. 1995).
Acknowledgments
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 sugar-bush for the study. Research was supported by USDA Special Grant 89-34157-4366 to M. T. T.
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