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Published online 2 February 2006
Published in J Environ Qual 35:433-441 (2006)
DOI: 10.2134/jeq2004.0347
© 2006 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
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TECHNICAL REPORTS

Heavy Metals in the Environment

Soil Acidity and Manganese in Declining and Nondeclining Sugar Maple Stands in Pennsylvania

Wilhelm J. Kogelmanna,* and William E. Sharpeb

a Department of Crop and Soil Science, Pennsylvania State University, 116 ASI Building, University Park, PA 16802
b School of Forest Resources and Penn State Institutes of the Environment, Pennsylvania State University, 136 Land and Water Building, University Park, PA 16802

* Corresponding author (wjk11{at}psu.edu)

Received for publication September 7, 2004.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
For decades, the hardwood forests of northern Pennsylvania have been subjected to chronic atmospheric loading of acidifying agents. On marginal, high-elevation, unglaciated sites, sugar maples (Acer saccharum Marsh.) have experienced severe decline symptoms and mortality. Accelerated soil acidification, base cation leaching, and increased availability of toxic metals have been suggested as predisposing factors contributing to this decline. Manganese, an essential micronutrient, is also a potentially phytotoxic metal that may be a factor associated with poor sugar maple health on soils vulnerable to acidification from anthropogenic sources. We measured Mn levels in four compartments of the soil–tree system (soil, foliage, xylem wood, and sap) on three sugar maple stands in northern Pennsylvania. Two stands were classified as declining and one was in good health. Negative correlations were found between soil pH and Mn levels in the soil, foliage, sap, and xylem wood. Levels of Mn in these pools were consistently higher on declining sites, which correspondingly exhibited lower levels of Ca and Mg. Species differences between red maple (Acer rubrum L.) and sugar maple at the two declining sites suggested different tolerances to excessive Mn. Molar ratios of Mg/Mn and Ca/Mn were different among sites and showed potential as indicators of soil acidification. Significant correlations among soil, sap, foliage, and xylem wood Mn were also noted. These results show clear Mn differences among sites and, when viewed with recent Mn toxicity experiments and other observational studies, suggest that excessive Mn may play a role in the observed decline and mortality of sugar maple.

Abbreviations: CEC, cation exchange capacity • ECS, exchangeable cation sum


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
HIGH-ELEVATION FOREST ECOSYSTEMS in northern Pennsylvania are receiving some of the highest loads of acidic deposition, relative to background conditions, in the USA (Lynch et al., 1995, 2000). Despite SO2 emission reductions resulting from the 1990 Clean Air Act Amendments, inputs of acidifying agents (SO42–, NO3–, NH4+, H+) persist well above background levels and, in northern Pennsylvania, are among the highest in the nation. Sustained exposure to acidic deposition may be changing the chemical environment of poorly buffered forest soils in Pennsylvania via accelerated leaching of base cations (Mg, Ca, and K) from both foliage and soil, accumulation of N and S, and increased solubilization and availability of potentially phytotoxic metals (Al and Mn) (Driscoll et al., 2001).

Sugar Maple Decline
Within this setting of chronic loading of acidifying agents is the phenomenon of sugar maple decline (Bauce and Allen, 1991; Drohan et al., 1999; Houston, 1999; Kolb and McCormick, 1993; McWilliams et al., 1996; Long et al., 1997). Decline refers to an irreversible, gradual deterioration of tree health resulting from a complex of biotic and abiotic causal factors that are conceptualized as predisposing, inciting, and contributing (Manion, 1991). Due to the complex array of stresses to which trees are exposed (e.g., extreme climatic events, drought, periodic defoliations, site conditions, competition, and pathogens), understanding the etiology of decline is difficult since predisposing factors that weaken trees may not ultimately be responsible for dieback and mortality. This uncertainty has resulted in debate regarding the role played by acidic deposition and soil acidification in observed sugar maple decline. Those who contend that acidic deposition is an important factor point out that it is unlikely that forest soils would fail to respond, in some way, to decades of sustained loading of acidifying agents (Robarge and Johnson, 1992; Hendershot and Jones, 1989; Sharpe et al., 1999). Moreover, the presence of mature sugar maple on declining sites indicates that, at some point in the past, conditions were amenable to colonization, stand establishment, and development. Stresses such as defoliation, drought, and pathogens are not novel, and trees would be expected to have the capacity to recover were they not predisposed by nutrient impoverishment and metal toxicity resulting from acidic deposition. Counter arguments suggest that sites where decline is occurring (i.e., high-elevation, unglaciated, nutrient-poor, upper-slope positions) are naturally unsuitable for sugar maples, and forest maturation may be causing increased susceptibility to defoliation, drought, and temperature extremes (Horsley et al., 2000; Houston, 1999). Additionally, there is evidence on some stands that repeated episodes of damage from drought and defoliations are responsible for reduced tree growth (Kolb and McCormick, 1993). Historical soil chemistry data are generally lacking, making determination of preindustrial soil chemical status difficult. Where historical soils data were available for the region, Drohan and Sharpe (1997) reported declines in exchangeable Ca and Mg.

Recent studies suggest a role of Mn in sugar maple health. In a study of 43 stands across northern Pennsylvania, Horsley et al. (2000) found sugar maple to be predisposed to decline by imbalanced Mg, Ca, and Mn nutrition. Drohan et al. (2002) studied 28 northern Pennsylvania sugar maple stands and noted significant foliar Mn and Mg/Mn (molar ratio) differences between declining and nondeclining sites. McQuattie and Schier (2000) exposed sugar maple seedlings grown in sand culture to various levels of Mn. Seedling mortality exceeded 90% at solution Mn levels of 40 mg L–1 and above, and at other treatment levels root and shoot dry mass decreased with increasing Mn. Moreover, a range of toxicity symptoms were noted, including fine root damage, induced Ca and Mg deficiencies, and foliar chlorosis and necrosis. Timmer and Teng (1999) applied vector diagnosis techniques to foliar chemistry and decline symptom data from four case studies and surmised that sugar maple decline may be linked to induced base cation deficiency caused by toxic Mn accumulation in the rooting zone. St. Clair and Lynch (2004, 2005) found high Mn treatments to impair photosynthetic function of sugar maple and red maple, especially under high light conditions. Furthermore, photosynthetic rate was negatively correlated with foliar Mn concentrations across all species studied.

Manganese in the Soil–Plant System
The plant availability of Mn, a common soil element as well as an essential micronutrient for plants, is highly sensitive to changes in soil acidity and reducing conditions (Barber, 1984). In well-oxidized soils, reducing conditions can be eliminated as a primary factor determining the availability of Mn to plants; therefore pH is the master variable. Labile Mn is defined as a rapidly responding Mn source or sink that is dependent on soil pH. As pH decreases, Mn oxides dissolve, increasing the concentration of Mn in the soil solution, on soil exchange sites, and on transport sites in root plasma membranes. If it is assumed that the number of ion-binding sites in the root plasma membrane is small relative to the number of ions in solution, pH decline would lead to a higher concentration of Mn in the uptake stream, since plants are unable to exclude unneeded ions from uptake (Marshner, 1995). Thus, soil pH decline may lead to elevation of both extractable Mn in the soil and biomass Mn. Manganese can be a toxic agent to plants through induced nutrient deficiencies, decreased photosynthesis, and reduced yield (Foy, 1984). There are multiple suspected mechanisms of Mn toxicity, and the tolerance of plants to excessive Mn varies both within and among species (Maas et al., 1968; Csatorday et al., 1984; Houtz et al., 1988; Morgan et al., 1976; Horiguchi, 1988). According to Foy (1984), Mn is probably the second most important growth-limiting factor, after Al, in acid soils. One mechanism of toxicity is a reduced uptake of cations of similar valence and ionic radius. Deficiencies of Ca, Mg, and Fe can thus be induced, and Mn toxicity can be expressed as deficiency symptoms of these nutrients.

Numerous studies have indicated that it may be the molar ratio of Mn to other elements (especially Mg, Ca, and Fe) that is critical in Mn toxicity (Lafond and Laflamme, 1968; LeBot et al., 1990; Ouellette and Dessureaux, 1985; Peaslee and Frink, 1969). Select molar ratios can be sensitive indicators of chemical changes in the soil environment due to acidification because of the different responses elements exhibit. For instance with soil acidification, base cations (Ca2+, Mg2+, and K+) may be depleted, while Al3+ and Mn2+ availability increases.

In this study, we present a unique data set that details Mn and other elements (Ca, Mg, K, Al, and Fe) in the soil, foliage, wood, and sap. These data were compared among three sites that differed in terms of soil acidity and sugar maple decline symptoms. The null hypotheses tested were: (i) there are not significant correlations between soil pH and Mn in soil, sap, foliage, and wood tissue; (ii) significant correlations do not exist among Mn levels in the four compartments of the soil–tree system studied (soil, sap, wood, and foliage); (iii) ratios of Mn to Ca, Mg, and Fe are not significantly correlated with soil pH in the pools studied and have no value as indicators of soil acidification; and (iv) Mn levels in soil, sap, wood, and foliage are not different between sites of differing sugar maple stand health.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Three northern hardwood stands dominated by sugar maple were chosen for this study (Table 1). Stands D4 and D6 are on the unglaciated Allegheny Plateau and stand IP is on the glaciated Allegheny Plateau (Fig. 1). All sites are located in Potter County, Pennsylvania, and contain trees of similar age and size [33 to 51 cm dbh (diameter at breast height)]. Historical data indicate that the stands in this region originated in the early 1900s due to extensive forest clearing (Whitney, 1990). Other tree species present on the study sites include black cherry (Prunus serotina Ehrh.), red maple, and American beech (Fagus grandifolia Ehrh.).


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  		Table 1. General summary of the three study sites.

 

Figure 1
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  		Fig. 1. Location of study sites in Potter County, Pennsylvania, USA.

 
The northernmost stand (IP) is located at an elevation of 600 m. The soil was mapped as a Culvers channery silt loam (a fine-loamy, mixed, superactive, frigid Oxyaquic Glossudalf; Goodman, 1958), a moderately well-drained, deep soil occurring on Wisconsinan glacial till. The O, A, and B horizons sampled had thicknesses of 4, 20, and 100+ cm, respectively. The IP stand was classified as a nondeclining stand based on basal area increment, crown size, and mortality in two studies of declining and healthy sugar maple stands (Swistock et al., 1999).

The D4 stand is located in the Susquehannock State Forest in the southern part of the county. This ridge-top site is at an elevation of 650 m. The soil is a Wharton channery silt loam (a fine-loamy, mixed, active, mesic Aquic Hapludult; Goodman, 1958), a moderately well-drained soil occurring on interbedded shale and sandstone of the Pocono formation. Thickness of the O, A, and B horizons sampled average 2, 15, and 101 cm, respectively. This stand was classified as declining by Sharpe and Sunderland (1995), who reported that 64% of sugar maples were dead.

The third site, D6, also in the Susquehannock State Forest, is a nearly level ridge top (650 m), 2.7 km from D4. The soil is a Leetonia stony loamy sand (a sandy-skeletal, siliceous, mesic Entic Haplorthod; Goodman, 1958), a coarse, rapidly permeable soil occurring on residuum derived from quartz conglomerate and sandstone of the Pocono and Pottsville formations. Thickness of the O, A, and B horizons average 2.5, 13, and 38 cm, respectively. The D6 stand was classified as declining by Sharpe and Sunderland (1995), with 47% of sugar maples dead.

Ten to 15 trees per stand, within a 1-ha area, were randomly selected for sampling of foliage, sap, and wood tissue. The same trees were used for all measurements. On the IP and D4 sites, sugar maple trees were sampled; and at D6, red maple trees were sampled. The D4 and D6 sites were replicate sites in the study of Sharpe and Sunderland (1995), so we sampled red maple on one of these (D4) to explore species differences. The O, A, and B horizon soil samples were collected from each site within 1 m of each study tree. Samples were taken from the walls of hand-excavated pits. Thus, each observation consisted of all the data for the local soil–tree system. Soil samples were dried, sifted through a 2-mm sieve, and extracted for plant-available nutrients using 0.01 M SrCl2, following the method of Joslin and Wolfe (1989). The supernatant was analyzed by atomic absorption spectroscopy to obtain values for Mn, Fe, Al, Ca, Mg, and K. Soil pH was determined in a 1:1 soil/water paste. Foliar samples were collected in late summer in 1995 (D4) and 1997 (D6 and IP). Since Mn is not reabsorbed by the tree, Mn accumulates steadily throughout the growing season (Lea et al., 1979; McCain and Markley, 1989); therefore, it is best to sample just before leaf senescence. Leaves were sampled from study trees using a shotgun to remove mid-canopy twigs. Leaves were then sealed in plastic bags and frozen for later analysis. Leaves were dry ashed at 490°C for 2 h and then dissolved in 1 M HCl. The solutions were analyzed for Mn, Ca, Mg, K, Fe, and Al by inductively coupled plasma (ICP) emission spectrometry.

Ten sugar maples from D4 and IP were tapped for xylem sap on four occasions from mid-March to mid-April 1998. The same trees were tapped on each occasion. The tapping technique was adapted from McCormick (1997). Tap holes were drilled at breast height with a stainless steel bit. The hole was flushed with deionized water and the tap was inserted. Tygon tubing was used to drain sap into 125-mL polyethylene bottles that were frozen for later analysis. Manganese, Ca, and Al concentrations were determined by atomic absorption spectroscopy.

Xylem tissue was sampled in 1997 and 1998. Cores were extracted using a Teflon-coated increment borer that was rinsed with acetone and deionized water before each use. Cores were extracted from locations adjacent to holes used to obtain sap. Cores represented 7 to 10 yr of conducting tissue, based on analysis under a dissecting microscope. If cores exhibited evidence of rot, they were discarded and a new core was taken from a different location. Dried and ground cores were dry ashed at 490°C for 4 h and then dissolved in 1 M HCl. The solutions were analyzed for Mn, Ca, Mg, K, Fe, and Al by ICP emission spectrometry.

Due to the relatively small sample sizes, nonparametric methods were utilized using Minitab version 13.1 statistical software (Minitab, State College, PA). To test for pairwise significant differences among sites, the Mann–Whitney test was used. For correlation analysis, Spearman's coefficient of rank correlation was used.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Table 2 summarizes the soil chemistry data for the O, A, and B horizons for all study sites. The O, A, and B horizons had pH values that were significantly different between the declining and nondeclining stands. The D4 and D6 stands had consistently greater acidity across all horizons compared to IP, but they did not differ from one another in pH of the O and A horizons, where the majority of feeder roots are located. Differences in exchangeable Al also indicated the degree of soil acidity, with the unglaciated (declining) sites exhibiting consistently greater exchangeable Al, most notably in the B horizon. In the O and A horizons, less Al would be expected to be exchangeable due to the ability of organic matter to bind Al (Taylor, 1988). Moreover, Al is not an essential nutrient, and thus it may be largely excluded from the uptake stream (Smith and Shortle, 1996), which would result in foliage, and consequently litter, with very low Al concentrations. Aluminum desorbed or released from minerals by the weathering action of H+ ions is considered an "acidic cation" that releases H+ ions during hydrolysis and cation exchange, thus contributing significantly to soil acidity.


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  		Table 2. Mean exchangeable soil cation data for the three study sites separated by soil horizon. Data based on 0.01 M SrCl2 extraction.

 
Cation exchange capacity (CEC) was approximated by summing the exchangeable cation charges. This was not a true CEC, since exchangeable H+ was not measured; however, the contribution of exchangeable H+ is typically small relative to Al in extremely and very acid soils. Recognizing this, we refer to this CEC approximation as exchangeable cation sum (ECS). On the declining sites, exchangeable Al accounted for a much larger fraction of the ECS than the nondeclining site. For example, in the A horizon, Al accounted for just 0.3% of the ECS at the IP site, while at the D4 and D6 sites, this value was 17 and 20%, respectively.

An examination of the soil profiles at both sites showed no evidence of mottling or poor drainage; therefore, it was concluded that Mn availability was not influenced by reducing conditions and that soil acidity was the factor controlling Mn availability. Exchangeable Mn, Ca, Mg, and K were significantly different between declining and nondeclining stands in nearly all instances (Table 2). While the declining stands exhibited many significant differences for exchangeable Mn, Ca, Mg, and K in the O and A horizons, the magnitude of these differences was smaller than those between the declining and nondeclining sites. Clearly, the declining stands were more nutrient impoverished. All sites had significantly different levels of exchangeable Mn in O horizons, with D4 and D6 O horizons at 16 and 73 times, respectively, the exchangeable Mn of IP. In the A horizon, D4 had more exchangeable Mn than D6 or IP, which were not different from one another. Exchangeable Mn in the B horizon showed clear differences between the declining and nondeclining sites. The prominence of Mn on the soil exchange complex for the declining sites compared with the nondeclining site is apparent when its contribution to the ECS is compared. In composite samples of O and A horizon soils, exchangeable Mn was 0.5% of the ECS on the IP site and 12 and 15% for D4 and D6, respectively.

Exchangeable Mn appears to decrease exponentially with decreasing acidity (Fig. 2). Figure 2 indicates a rapid decline in exchangeable Mn as pH approached 4.2, where it appeared to level off. All sites showed decreasing exchangeable Mn with increasing soil depth. This may be attributed to the soil's capacity to adsorb Mn as soil water is moving down the profile. Moreover, pH increased with soil depth, which could have rendered some Mn unavailable. An O horizon rich in Mn is due to decay of plant matter with high Mn concentrations.


Figure 2
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  		Fig. 2. Scatter plot of mean OA horizon pH and mean OA horizon 0.01 M SrCl2 extractable Mn for all three study sites. Spearman's nonparametric coefficient of rank correlation ({rho}) indicates a highly significant negative correlation.

 
Much greater amounts of exchangeable Ca and Mg were measured on the IP site than on D4 or D6. This may be a function of differing parent material and age of the soils, with the glaciated IP site having been exposed to much less weathering and base cation leaching. Additionally, it indicates a lower acid buffering capacity on the D4 and D6 sites. Whether the declining sites had experienced accelerated base cation leaching and soil acidification as a result of acidic deposition remains unknown, although some researchers posit this as a predisposing factor in sugar maple decline (Hendershot and Belanger, 1999). The less acidic nature of the IP soil may have immobilized Mn as solid oxides. Calcium and Mg do not have the tendency to switch between solid and solute phases as readily as Mn, and therefore the low values at D4 and D6 may have indicated leaching losses that were not compensated by mineral weathering or release from organic material. Manganese exchanges readily with Ca, Mg, and monovalent cations (Norvell, 1988). Divalent transition metals are often sorbed as inner-sphere complexes and are more strongly sorbed than alkaline earth metals such as Ca and Mg (Sparks, 1995). Thus Mn may have exacerbated base cation leaching losses from the more acidic sites.

The data for K shows trends similar to Ca and Mg for the mineral horizons (A and B). In the O horizon, however, the IP site was not statistically different from D4, but D6 was significantly higher than both. Potassium is rarely mentioned as a nutritional variable of concern in the literature; however, Drohan et al. (2002) did note significant differences in foliar K among declining and nondeclining stands in Pennsylvania. Ouimet and Fortin (1992) showed lower foliar K to be linearly related to growth and canopy condition of sugar maples. Additionally, K uptake can be suppressed when soil Ca and Mg are high, as was the case with the IP site. Our foliar data (Table 4) indicate that all stands were generally within the K range for healthy trees, although D4 and D6 were on the low end of that range (Kolb and McCormick, 1993).


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  		Table 4. Mean foliar chemistry and selected molar ratios for the three sites sampled.

 
In considering relative element availability using molar ratios (Table 3), higher Ca/Al ratios were found on the IP site. Researchers have found a Ca/Al ratio <1 in the soil solution to be a threshold for plant growth effects (Cronan and Grigal, 1995; Thorton et al., 1987). Although the Ca/Al ratio was well above unity for all sites in the O and A horizons, the data indicate the potential for Al to play a prominent role in the soil on the more acidic sites. This could indicate the possibility of Al-related stresses such as fine root damage and inhibition of base cation uptake; however, it must be noted that this ratio was largely driven by Ca differences, since the magnitude of differences in Al were rather small. In the B horizon, the declining sites had Ca/Al ratios <1. Such a ratio may be deleterious to roots at this depth, limiting their ability to extract water, which could be a source of stress during dry periods when the surface soils have low available moisture. Furthermore, roots concentrated in the surface horizons are more dependent on tight nutrient cycling, susceptible to freezing injury, and may be more at risk from wind throw.


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  		Table 3. Mean molar ratios of exchangeable cations based on 0.01 M SrCl2 extraction of soil samples. Standard error of the mean shown in parentheses.

 
The Mg/Mn and Ca/Mn data tell a more interesting story of the nutrient balance in the soils (Table 3). A large and statistically significant separation was observed, with the IP site having much higher ratios than D4 and D6. For instance, the Ca/Mn ratio of the IP soil was 630, 241, and 324 for the O, A, and B horizons, respectively, whereas the D4 site had values of 5.9 (O horizon), 7.0 (A horizon), and 5.8 (B horizon). These results suggest possible Mn interference with uptake of Ca and Mg. Interference at uptake sites in the root systems was likely, with the possibility that deficiencies of base cations could be induced (Marshner, 1995; Heenen and Campbell, 1981). Further, Mn may be less susceptible to leaching than other cations. There is evidence that Mn is bound preferentially over Ca. Norvell (1988) reported Mn being adsorbed in the presence of large quantities of Ca2+ and added that there were fractions of soil Mn that were difficult to replace except by other transition metals or strong chelating ligands.

The foliar elemental concentrations (Table 4) are reflective of the soil data. Again, declining sites were associated with higher Mn values. In fact, foliar Mn concentrations for D4 (sugar maple) and D6 (red maple)-with means of 2535 and 4512 mg kg–1, respectively-were among the highest reported in the literature. Foliar Mn at the IP site was significantly lower, with a mean of 481 mg kg–1, but this was within the range for adequate tree nutrition (Kolb and McCormick, 1993). When the OA horizon mean Mn was expressed as a fraction of ECS (data not shown), D4 and D6 did not differ significantly. These data suggest that red maple may have the capacity to accumulate greater amounts of foliar Mn, perhaps without adverse consequences. In liming experiments with seedlings grown on native soils, St. Clair (2004) found sugar maple to be photosynthetically more responsive to liming treatments than red maple and that the increased photochemical capacity may have been the result of improved Mg nutrition, amelioration of Mn toxicity, or both. Widespread expansion of red maple has been noted in eastern forests (Abrams, 1998), with tolerance of nutrient-poor soils considered a factor in its success. We noted an abundance of red maple seedlings on the D6 site and a paucity of sugar maple seedlings, although no data were collected to quantify this observation.

Foliar Mn levels at D4 was similar to those in declining stands studied by Kolb and McCormick (1993), Horsley et al. (2000), and Drohan et al. (2002) and exceeded those associated with seedling mortality in Mn toxicity studies by McQuattie and Schier (2000). The results of McQuattie and Schier (2000) suggest that mature trees may have greater tolerance than seedlings to elevated Mn. This may contribute to regeneration problems and eventual replacement by more tolerant species such as red maple.

The IP site had foliar Ca, Mg, and K concentrations that were significantly higher than those at D4 and D6, reflecting the concentrations of these elements in the soil (Table 1). High inputs of acid anions and H+ may have been responsible for accelerated base cation leaching at the declining D4 and D6 sites. The foliar Ca and Mg concentrations on the D4 and D6 sites were low compared with ranges reported in the literature (Table 4), implying that the availability of these elements may have been limiting. Liming studies on nearby sites with similar soils showed positive growth responses by sugar maple (Long et al., 1997).

Trends for molar ratios in the foliage reflected those in the soil. The Mg/Mn, Ca/Mn, and Fe/Mn ratios signaled substantial differences in the nutrient balances between the trees on the more and less acidic sites. In all cases, the IP site had significantly higher ratios. These foliar concentrations could have ramifications for the C balance of the tree, since Mg and Fe are vital to the photosynthetic apparatus. In studies of Mn toxicity in tomato (Lycopersicon esculentum Mill.) and wheat (Triticum aestivum L.), LeBot et al. (1990) found foliar Mg/Mn concentrations to be a better indicator of toxicity onset than Mn concentration alone, and growth relative to controls declined as the Mg/Mn ratio fell below 1. With an average ratio of 9.23, our data showed the IP foliage well above this level, while the declining sites had values <1.

High foliar Mn concentrations could imply possible Mn toxicity, although toxic thresholds are not known for the species studied. Excessive Mn in the foliage has been associated with decreased net photosynthesis (St. Clair, 2004; St. Clair and Lynch, 2005; Houtz et al., 1988), inhibited chlorophyll synthesis (Csatorday et al., 1984), and chlorotic and necrotic spotting (Pickens 1995). It is possible that the relatively large amounts of soil Ca and Mg were preventing excessive Mn accumulation in the foliage on the IP site, whereas trees on the D4 and D6 sites had no such moderating factor and were therefore accumulating large amounts of Mn.

Manganese content of xylem tissue was significantly different among all sites (Table 5). The D4 xylem tissue had the highest mean Mn content (369 mg kg–1)-more than seven times that of the IP site and twice that of D6. The wood tissue differences between D4 and D6 may indicate species differences. Significant differences between declining and nondeclining stands were detected for Ca in xylem tissue. Calcium at the D4 and D6 sites averaged 880 and 773 mg kg–1, respectively, while on the IP site the wood Ca was 4758 mg kg–1. Again, the chemical properties of the soil were expressed in the biomass. This was not the case for Al, where differences between sites were not significant. Xylem tissue Mg at the IP and D4 sites did not show significant differences, despite differences in the soil and foliage. Red maple (on D6) wood tissue, however, did reflect soil differences for Mg, which suggests a species difference.


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  		Table 5. Mean values for xylem wood chemistry for the three sites sampled.

 
Our results affirm those of DeWalle et al. (1991) and Hutchinson et al. (1998), who studied the relationship of sapwood chemistry to soil, leachate, and foliar chemistry. Watmough (2002) contended that if a relationship between growth and tree ring chemistry is identified, then dendrochemistry may provide a cost-effective means of identifying areas currently at risk from acidic deposition. While our data do not directly link xylem tissue chemistry to tree health, it shows potential as an indicator of soil chemistry differences among sites (Tables 7 and 8).


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  		Table 7. Spearman's rank correlation for soil pH and Mn levels in the soil (exchangeable fraction), foliage, wood, and sap of sugar and red maples on the sites studied.

 

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  		Table 8. Spearman's rank correlation for soil pH and Mg/Mn molar ratios in the soil, foliage, and wood of sugar and red maples on the sites studied.

 
Absolute cation concentration trends may be less meaningful than changes in cation ratios in detecting the impact of changes in soil acidity (Bondietti et al., 1989). Xylem wood molar ratios of Mg/Mn, Ca/Mn, and Fe/Mn exhibited trends similar to comparable ratios in the soil and foliage. These results support the potential use of xylem tissue molar ratios as indicators of the effects of soil acidity changes. For example, Fig. 3 indicates the separation among declining and nondeclining sites based on wood Mg/Mn ratios. Spearman's rank correlation statistic indicated significant positive correlation between soil pH and the natural log of the Mg/Mn ratio of xylem tissue (Fig. 3). DeWalle et al. (1999), in an experimental watershed acidification study, determined that Ca/Mn and Mg/Mn ratios were superior to Ca/Al ratios in sensitivity to changes in soil acidity and found them to be effective indices of cation mobilization, more so than Ca, Mg, or Mn concentrations alone.


Figure 3
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  		Fig. 3. Plot of natural-log-transformed wood tissue Mg/Mn against mean OA horizon pH for the three study sites. Sites are distinguished with different point symbols. Spearman's nonparametric coefficient of rank correlation ({rho}) indicates a significant positive correlation.

 
Xylem sap analysis provides a snapshot of the nutrient-supplying potential of the soil–root system. Sap chemical content has been used to evaluate fertilizer additions, follow soil pollutants, and differentiate among contrasting soils (Stark et al., 1985; Stark and Spitzner, 1985). Sap was collected on 4 d in March and April 1998 from the stands where sugar maples were sampled (D4 and IP). Data are presented for one tapping occasion (Table 6), but the same trends were observed on all days. A comparison of early- and late-season sap data indicated increasing Mn concentration with time (data not shown). Increasing sap nutrient concentrations preceding bud burst have been noted by other researchers (Stark and Spitzner, 1985). Sap from sugar maples on the D4 site exhibited significantly greater Mn. This fit the same pattern as the soil, wood, and foliar data and indicated that these Mn pools were generally reflective of one another (Table 7). Differences in sap Ca concentrations were significant between sites, with the IP site having the higher values; this observation fit the pattern observed in the soil, wood, and foliage. Aluminum was also different, with the IP having the higher values; however, both sites were <1 mg L–1. Low sap Al was probably the result of an Al-exclusion mechanism in the root cortex. The IP site had higher molar ratios of Ca/Al and Ca/Mn in the sap. Our data indicate that sap reflects differences in the soil chemical environment between declining and nondeclining sugar maple stands and that molar ratios of Ca/Mn are a better indicator than Ca/Al.


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  		Table 6. Mean values for xylem sap chemistry for the IP and D4 sites where sugar maples were sampled.

 
The soil, sap, foliage, and wood chemistry data showed that marked differences existed between the declining and nondeclining sites in terms of Mn, Ca, Mg, K, Al, and selected molar ratios. Additionally, elemental concentrations in the biomass (foliage, wood, and sap) were reflective of the extractable soil fraction.

Correlations between Mn in the soil (exchangeable), foliage, sap, and wood and soil pH are summarized in Table 7. Correlation of ranks (which include data pooled from all sites) is significant in all cases, which indicates increasing Mn in all pools as pH decreases. Manganese levels in the soil are correlated with Mn in the sap and biomass, which in turn are correlated with each other. The Mg/Mn cation ratios also show significant correlations for soil pH and among the foliage, soil, and xylem tissue (Table 8). The Mg/Mn ratio has the strongest correlations with soil pH and among the three compartments sampled (Mg was not measured in sap). The Mg/Mn ratio may be superior to Ca/Al for detection or monitoring of forest soil chemistry changes resulting from acidic deposition.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
Results from this study indicate that significant inverse correlations existed between soil pH and Mn levels in the sap, soil, foliage, and wood tissue for the study trees. Levels of Mn in the extractable soil fraction, sap, foliage, and wood were significantly different between declining and nondeclining sites. The Al concentrations in sugar and red maple foliage and wood tissue were not a reliable indicator of soil acidity. Results invalidate the use of Ca/Al ratios in foliar and wood tissue analysis because the ratio is primarily Ca dependent and trees are not taking up appreciable quantities of Al. The Mg/Mn or Ca/Mn ratios are suggested as better indicators. Molar ratios of Mg/Mn, Ca/Mn, and Fe/Mn show promise as indicators of soil acidity conditions for the pools studied. Results also suggest that excessive levels of soil Mn may be contributing to low soil and foliar concentrations of base cations on declining sugar maple sites. Moreover, Mn may have played a role in the poor health and mortality of sugar maple on these sites either through direct toxicity within the foliage or through induced base cation deficiencies. Species differences in foliar Mn between red and sugar maples indicate that red maple is accumulating larger quantities of Mn, apparently without adverse consequences.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 





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Vadose Zone Journal Journal of Plant Registrations
Journal of Natural Resources
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