Relationship of understory diversity to soil nitrogen, topographic variation, and stand age in an eastern oak forest, USA

Forest Ecology and Management 217 (2005) 229–243 www.elsevier.com/locate/foreco

Relationship of understory diversity to soil nitrogen, topographic variation, and stand age in an eastern oak forest, USA Christine J. Small a,*, Brian C. McCarthy b b

a Department of Biology, Radford University, P.O. Box 6931, Radford, VA 24142, USA Department of Environmental and Plant Biology, Ohio University, Athens, OH 45701, USA

Received 25 February 2005; received in revised form 3 June 2005; accepted 7 June 2005

Abstract Nitrogen (N) availability is a primary limiting factor in many temperate deciduous forests. However, increased atmospheric N deposition over recent decades has dramatically altered nutrient cycles in many eastern forests. Given the variability of ecosystem responses to N deposition and the sensitivity of herbaceous layer vegetation to edaphic and microenvironmental conditions, changes in nutrient dynamics could have important implications for forest diversity and productivity. To better understand variations in soil N relative to understory dynamics, we sampled herbaceous layer composition and diversity across topographic gradients in managed (10-year-old aggrading) and mature (>125 years) mixed-oak stands in southeastern Ohio. Vegetation was sampled in spring and summer to capture variations in vernal and late season herb communities. Edaphic and microenvironmental conditions were characterized during these same periods, including analyses of upper mineral soil samples for total C, N, and C/N ratio. Aggrading stands showed significantly lower soil N than mature forest stands (spring = 0.145% versus 0.165%; summer = 0.146% versus 0.197%; P < 0.001). Topography influenced soil N, with greater availability on lower and north-facing slopes (P < 0.05). Across all stands, C/N was strongly correlated with herb layer composition (spring r = 0.606; summer r = 0.449) and, in mature stands, was a strong predictor of understory richness (linear regression; r2 = 0.634; P < 0.001), particularly on poorer sites. These results emphasize that changes in soil and vegetation with increased N deposition are likely to be site-specific, even within relatively uniform systems. Understory diversity patterns on less fertile sites or in more mature forests, those systems exhibiting strongest correlations with soil C/N ratios, appear most likely to be affected, whereas edaphic limitations in vigorously growing, aggrading vegetation may be less impacted. Because herbaceous layer interactions are tightly linked to ecosystem-level nutrient dynamics and to woody seedling success, these influences have the potential to significantly alter overstory recruitment patterns and broader ecosystem responses to N deposition. # 2005 Elsevier B.V. All rights reserved. Keywords: Herbaceous layer richness; Clearcut harvesting; Forest management; Soil carbon:nitrogen; Nitrogen saturation

* Corresponding author. Tel.: +1 540 831 5146. E-mail address: [email protected] (C.J. Small). 0378-1127/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2005.06.004

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1. Introduction A characteristic and vital component of eastern deciduous forests is the diversity of understory herbaceous vegetation (Braun, 1950; Muller and Bormann, 1976). The distribution and abundance of understory species in these systems has been correlated with a variety of historical factors (Foster et al., 1998) and complex environmental gradients, especially those related to topography (Cantlon, 1953; Huebner et al., 1995), light availability and canopy structure (Beatty, 1984; Collins et al., 1985), and soil moisture and fertility (Siccama et al., 1970; Hutchinson et al., 1999). The sensitivity of herbaceous species to these site quality conditions has led to their use as indicators of landform characteristics, disturbance history, and altered edaphic and environmental conditions across the landscape and over time (e.g., Pregitzer and Barnes, 1982; Meilleur et al., 1992). However, studies of vegetation dynamics in eastern forests have focused historically on larger and more economically important overstory species (e.g., Bormann and Likens, 1979; Muller, 1982), leaving patterns of herbaceous diversity poorly understood (Duffy and Meier, 1992; Gilliam et al., 1995; Small and McCarthy, 2003), particularly relative to disturbance and anthropogenic stresses. Nitrogen (N) availability is a primary limiting factor in many forests of eastern North America and other terrestrial ecosystems throughout the world (Aber et al., 1989; Tamm, 1991). However, human activities have greatly altered global N cycles, more than doubling inputs of atmospheric N to some terrestrial ecosystems (Vitousek et al., 1997). Over recent decades, forests of eastern North America have experienced marked increases in atmospheric N deposition resulting from industrial and agricultural pollution emissions (Aber et al., 1989; Galloway et al., 1995). Today, a number of these forests exhibit symptoms of N saturation (Fenn et al., 1998), the availability of ammonium (NH4+) and N oxides (especially NO3
) in excess of biological demand and biotic and abiotic retention capacities (Aber et al., 1989, 1998). These systems show reduced N limitation of vegetation and soil microorganisms and increased soil nitrate mobility. Once highly efficient at retaining N, these stands now export large quantities of nitrates over extended periods of time, resulting in

altered nutrient cycles, increased soil acidification and base cation leaching (particularly Ca2+), Al toxicity, and watershed eutrophication (Aber et al., 1989; Johnson and Taylor, 1989; Adams and Eagar, 1992; Vitousek et al., 1997). Nitrogen deposition continues to increase throughout much of eastern North America (Galloway et al., 1995), suggesting that saturation of terrestrial ecosystems may become more widespread. This form of N enrichment appears to have significant impacts on vegetation dynamics, particularly forest productivity, susceptibility to disturbance and secondary stressors (e.g., insect pests, disease, climatic extremes) and growth of ‘‘sensitive’’ species, such as forest herbs (Freidland et al., 1984; Johnson and Taylor, 1989; Bobbink et al., 1998). Current impacts of anthropogenically induced N deposition make it essential to better understand correlations between N availability and forest dynamics. A number of ‘‘predisposing’’ factors, those influencing the ability of forested systems to retain inputs of atmospheric N, have been identified, including vegetation type, successional stage, landuse history, topography, and edaphic conditions (Fenn et al., 1998; Goodale and Aber, 2001). This variation in ecosystem response to N deposition, coupled with the sensitivity of understory vegetation to nutrient gradients, suggest that changes in nutrient dynamics may strongly influence forest structure and diversity. Therefore, in an attempt to identify herbaceous communities and site conditions particularly responsive to soil N dynamics, we examined seasonal variations in understory diversity relative to soil N, C, and C/N ratio along topographically induced gradients in a central Appalachian deciduous forest, a region currently receiving high levels of N deposition (e.g., 15–20 kg ha
1 year
1 at Fernow, West Virginia (Gilliam et al., 1996; Fenn et al., 1998). The C/N ratio of the forest floor is considered to be a strong indicator of the degree of N limitation or saturation in forested systems (Van Miegroet et al., 1990; Currie, 1999) and often correlated with N mineralization rates and nitrate export (Hart et al., 1994; Williard et al., 1997). As managed forests comprise a large proportion of our eastern landscape and stand age and vigor are important influences on forest productivity, nutrient retention, and diversity (Bormann and Likens, 1979), we further examined understory vegetation and soil N relative to forest age following management.

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2. Materials and methods 2.1. Field and laboratory methods Field sampling was conducted at the Waterloo Wildlife Research Station (WWRS; 398210 800 N, 828160 5700 W), a 505 ha state-owned natural area in the Low Hills Belt section (Braun, 1950) of the Unglaciated Allegheny Plateau in Athens County, Ohio, USA (Fenneman, 1938). The topography of the study site is highly dissected, with moderate to steep slopes (20–70%) and ridgetops generally reaching elevations of 280–320 m. The climate is temperate continental, with mean annual precipitation of 102.5 cm relatively evenly distributed throughout the year (NCDC/NOAA, 1999). Soils of upper slopes and ridgetops are primarily classified as mesic Ultic and mesic Aquic Hapludalfs, consisting of moderately deep to deep, moderately well-to-well-drained silt loam surface soils and loam, silty clay loam, or silty clay subsoils, formed in residuum or from local colluvium of interbedded shale, siltstone, sandstone, and limestone (Lucht et al., 1982). Soils of lower slopes are typically Typic Dystrochrepts, with moderately deep-to-deep, well-drained loam or silt loam surface soils with loam or silty clay loam subsoils, formed in sandstone residuum (Lucht et al., 1982). The vegetation of WWRS lies within the mixed mesophytic forest association, a component of the unglaciated eastern deciduous forest region of Braun (1950). Mature forests are dominated by closed-canopy mixed-oak (Quercus spp.) or oak-hickory (QuercusCarya spp.) forests on drier sites and mixed mesophytic forests (e.g., Fagus grandifolia, Acer saccharum, and Tilia americana) on more mesic sites (Small and McCarthy, 2002). By the late 1800s and early 1900s, much of the region, including WWRS, was under cultivation or pasture and large areas experienced heavy timber harvesting (Gordon, 1969). Today, the overstory at WWRS is relatively even-aged and generally >125 years of age. These relatively mature stands are dominated by Acer rubrum, Quercus prinus, Quercus alba, Quercus velutina, Quercus coccinea, Fagus grandifolia, and Nyssa sylvatica. Young revegetating clearcut stands are also present, with similar dominance of A. rubrum and Q. prinus but greater importance of Liriodendron tulipifera, Prunus serotina, and Sassafras albidum (Small and McCarthy, 2002).

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In March 1998, permanent 2.5 m2 circular sample quadrats were established in six upland naturally revegetating clearcut stands (7 years; late stand initiation stage; Oliver and Larson, 1990) and six mature second-growth forest stands (>125 years; understory reinitiation stage; Oliver and Larson, 1990). Each of the 12 stands was approximately 1.75 ha in area (minimum dimensions 100 m  175 m) and uniformly treated (entirely clearcut or uncut). Pairs of clearcut and mature forest stands (statistical blocks) were located adjacent to one another (with buffer zone) or in relatively close proximity and were of similar elevation, slope, and aspect to minimize natural variability and allow examination of species–site relationships. Sixteen replicate quadrats were located within each stand in a stratified-random arrangement, with eight quadrats on upper slope positions and eight on lower slope positions (n = 192). Upper slope quadrats were located approximately one-third the distance from ridge-top to valley-bottom; lower slope quadrats were located approximately one-third the distance from valleybottom to ridge-top, within the boundaries of clearcut or mature forest treatments. At this study site and other north-temperate areas of moderate to high relief, topographic aspect has been shown to produce marked differences in soil moisture, fertility, and depth, corresponding to variations in herbaceous layer composition and diversity (e.g., Cantlon, 1953; Franzmeier et al., 1969; Small and McCarthy, 2002). Therefore, the topographic aspect (direction of slope face) was determined for each 2.5 m2 quadrat, allowing each to be assigned to one of three topographic aspect categories. These aspect categories were as follows: NE quadrats = 345.5–104.58 aspect (a 1198 range around due NE (458)); SW quadrats = 165.5–284.58 aspect (a 1198 range around due SW (2258)); intermediate (INT) quadrats = 105–1658 and 285–3458 aspect (each 608 ranges around due SE (1358) and NW (3158)). This resulted in six aspect/stand age classes: NE mature forest (n = 28), INT mature forest (n = 27), SW mature forest (n = 41), NE revegetating clearcut (n = 29), INT revegetating clearcut (n = 34), and SW revegetating clearcut (n = 33). In each quadrat, percentage cover of all herbaceous vascular plant species was estimated visually to the nearest 1%. Because herb composition and abundance varies seasonally, herbaceous quadrats were sampled

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in late April 1998 to capture peak growth of spring ephemerals and in late June 1998 for peak growth of graminoids and composites. Quadrats were revisited as necessary for species identification; nomenclature follows Gleason and Cronquist (1991). Samples of the upper 10 cm of mineral soil (A-horizon), the horizon containing the greatest concentration of herbaceous plant roots, were collected from each quadrat in late April and June of 2000 to correspond with spring and summer herb samples. Soil samples were dried to a constant weight at 100 C for 48 h and sieved using a 0.5 mm screen. Samples were analyzed by dry combustion for total N and C contents (C (%), N (%), and C/N ratio) using a CNS Macro Elemental Analyzer (Elementar Americas, Inc., Vario MAX, Mt. Laurel, New Jersey, USA). Additional soil texture, elemental nutrient, and moisture characteristics were determined from composite A-horizon samples collected in June 1998 from each quadrat. Overstory vegetation characteristics, understory light availability, temperature, relative humidity, leaf litter depth, and soil compaction also were measured in late April and late June of 1998 in each quadrat. (Data collection for additional measurements given in Small and McCarthy, 2002.) 2.2. Data analysis Mean cover and frequency were calculated for each herbaceous species in spring and summer aspect/stand age classes. Relative importance (RIV; 0–100%) was calculated as the average of relative cover (0–100%) and relative frequency (0–100%). Diversity of understory vegetation in clearcut and mature forest quadrats was assessed by calculating mean (per quadrat) and total (across all quadrats) species P richness and Shannon–Wiener diversity (H0 =
pi ln pi, where pi is the proportion of individuals found in the ith species; Magurran, 1988). Mean soil C, N, and C/N and herbaceous cover, richness, and H0 diversity were each evaluated using three-way repeated measures analysis of variance (ANOVA) tests to examine the effects of harvesting (clearcut versus mature forest; fixed effect), slope position (upper versus lower; fixed effect), topographic aspect (NE, INT, SW; fixed effect), and sampling period (April versus June; repeated measure, fixed effect; Sokal and Rohlf, 1995). Stand was treated

as a random effect and all interaction terms were included in each ANOVA model. Variables were transformed as necessary (log10) to meet ANOVA normality and homogeneity of variance assumptions. Significant results were compared using a posteriori Bonferroni multiple comparison tests. Analyses were performed using NCSS, 2000 (Hintze, 2000). The relationship of spring and summer herb layer composition to environmental variables was examined using Canonical Correspondence Analysis (CCA; PCORD software (McCune and Mefford, 1999)). CCA is a direct ordination technique that provides simultaneous evaluation of vegetation and environmental data (ter Braak, 1986). Environmental variables included in the preliminary CCA analysis were quadrat aspect, slope angle, litter layer depth, temperature, relative humidity, spring and summer open sky, and soil C, N, C/N, NO3, P, K, Ca, Mg, Al, moisture, organic matter, silt, clay, pH, and compaction (see Small and McCarthy, 2002 for variable means and comparisons among stands). Measured, quantitative aspect values for each quadrat were cosine transformed to values ranging from 0 (SW) to 2 (NE) for use in CCA (Beers et al., 1966). Abundance values for tree basal area and density, sapling cover and density, and seedling cover in the area surrounding each quadrat (see Small and McCarthy, 2002) were also included in the initial CCA analyses. Variables were log10 transformed to reduce the influence of outliers and to provide greater weight to changes in resource availability (particularly soil nutrients) at low concentrations (Palmer, 1993). Highly correlated variables and those only weakly associated with the first three axes were removed from subsequent analyses to produce the most parsimonious ordinations, in accordance with ter Braak (1986) and Palmer (1993). The relationship of understory richness and cover to C, N, and C/N ratio were examined for each sample period and aspect/age class using least squares regression analysis (Hintze, 2000). Mean richness and cover values per quadrat were log10 transformed to meet normality and variance assumptions of regression models. The relationships of these variables were compared across all sampled quadrats and between each of the three aspect classes for both clearcut and mature forest stands. Slopes of significant richness or cover versus C/N regression lines were compared using a modified analysis of covariance as described by Sokal and Rohlf (1995).

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3. Results 3.1. Edaphic and microsite conditions Percent N and C/N ratios varied with stand age throughout the growing season. In both spring and summer samples, N content was significantly lower in aggrading clearcut relative to mature forest soils (spring N = 0.15% versus 0.17%; summer N = 0.15% versus 0.20%; P < 0.001) and C/N ratios significantly higher (spring C/N = 16.12% versus 13.91%; summer C/N = 16.85% versus 14.54%; P < 0.001). Soil C did not differ with stand age or sampling season. A related study of these sample quadrats found significant differences in other microsite variables, with greater soil compaction, temperature, and spring light availability and lower soil clay content, leaf litter depth, and summer light availability in clearcut versus mature forest samples (all P < 0.01 except clay P < 0.05; Small and McCarthy, 2002). In spring, soil C and N varied with topographic position, with greater C and N on INT and NE aspects (P < 0.05 except spring clearcut SW versus NE, C not significant (ns); Fig. 1). Conversely, C/N ratios were higher on SW relative to NE and INT aspects (P < 0.01, spring and summer; Fig. 1). Soil C and N also varied with slope position (upper versus lower), both greater on lower slopes (P < 0.001; spring and summer samples; Fig. 2). C/N ratios did not differ with slope position. Other edaphic conditions correlated with aspect position included greater soil moisture, nutrient availability (especially, Ca, K, and Mg), Ca:Al ratios, and organic, and clay contents on NE (versus SW) clearcut quadrats and NE and INT (versus SW) mature forest quadrats (P < 0.001, all comparisons; Small and McCarthy, 2002). 3.2. Understory diversity and compositional patterns In spring, all measures of herbaceous abundance and diversity were significantly greater in clearcut relative to mature stands, including mean cover (10.94  1.42 versus 4.89  0.57), richness (6.03  0.41 versus 4.71  0.45), and H0 diversity (1.34  0.07 versus 1.08  0.09; P < 0.01 all comparisons). Similar but statistically insignificant trends were observed in summer samples. Total herb richness

Fig. 1. Comparison of mean soil C (%), N (%), and C/N ratio in 192 sample quadrats on NE, INT (NW/SE), and SW topographic aspect positions during spring (April) and summer (June) sample periods. Bars represent one standard error.

was greater in younger (clearcut) stands during both sample periods, with little seasonal change (spring herb richness = 68 versus 59; summer = 69 versus 57). Abundance of herbaceous species varied significantly with aspect position in mature stands, with greater mean cover on INT relative to NE and SW aspects. Clearcut stands showed a similar non-significant trend (Fig. 3). Herb diversity also varied significantly with slope aspect, with greater mean richness and H0 diversity on INT and NE aspects relative to SW (P < 0.0001 except H0 in SW versus NE summer clearcut, ns; Fig. 3). Likewise, total richness was greater in INT forest and NE and INT clearcut quadrats. Slope position (upper versus lower) significantly influenced herb richness, with greater richness on lower slopes in both stand types and sample periods (P < 0.0001; results not shown). Clearcut and mature forest quadrats shared importance of several herbaceous species, including

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Fig. 2. Comparison of mean soil C (%), N (%), and C/N ratio in 192 sample quadrats at upper and lower slope positions. Bars represent one standard error. Asterisks indicate significant differences between upper and lower slope means (P < 0.05).

Aster divaricatus, Aster lateriflorus, Amphicarpaea bracteata, Carex digitalis, Lysimachia quadrifolia, Polysticum acrosticoides, Potentilla simplex, and Viola sororia (Table 1). Through the growing season, younger stands showed greater importance of annual or shade-intolerant graminoids, such as C. digitalis, Carex laxiflora, Panicum clandestinum, and Poa spp. and non-native herbs (e.g., Cardamine hirsuta and Potentilla recta), whereas mature stands showed greater importance of shade-tolerant perennials, including Cimicifuga racemosa, Osmorhiza claytonii, Polygonatum pubescens, Smilacina racemosa, and Uvularia perfoliata. Two N-fixing leguminous species, Desmodium glutinosum and A. bracteata, were also more abundant in mature stands. Seasonal preferences were evident in Boehmeria cylindrica,

Fig. 3. Comparison of mean herb cover (%), Shannon–Wiener diversity (H0 ), and richness and total herb richness in 192–2.5 m2 quadrats on NE, INT (NW/SE), and SW aspect positions during spring (April) and summer (June) sample periods. Bars represent one standard error.

Cardamine concatenata, Geranium maculatum, and Podophyllum peltatum in spring and D. glutinosum in summer (Table 1). 3.3. Understory–site relationships Canonical Correspondence Analysis (CCA) of spring herb layer and site data showed marked

C.J. Small, B.C. McCarthy / Forest Ecology and Management 217 (2005) 229–243 Table 1 Importance values (RIV; 0–100%) of herbaceous layer species in sample quadrats Species

Amphicarpaea bracteata Aster divaricatus Aster lateriflorus Boehmeria cylindrical Cardamine concatenata Carex digitalis Carex laxiflora Cimicifuga racemosa Desmodium glutinosum Galium aparine Geranium maculatum Geum canadense Lysimachia quadrifolia Osmorhiza claytonii Panicum clandestinum Poa sp. Podophyllum peltatum Polygonatum pubescens Polysticum acrosticoides Potentilla simplex Smilacina racemosa Uvularia perfoliata Viola sororia

Spring

Summer

Clearcut

Forest

Clearcut

Forest

2.35 5.91 6.12 – – 12.61 3.50 – – 5.15 3.87 – 2.29 – 3.80 3.19 2.79 2.34 3.38 9.25 – – 3.29

5.34 5.01 4.02 3.42 2.88 4.05 3.05 4.00 – 4.24 3.91 2.66 2.88 3.53 – 3.32 2.26 4.67 5.18 4.87 2.50 2.51 3.38

3.26 5.15 6.99 – – 12.05 6.01 – 5.96 – – – 3.60 – 3.67 2.05 – – 4.74 8.96 – – 3.99

4.36 4.54 2.75 – – 2.48 – 5.00 14.36 5.12 2.49 – 2.89 2.00 2.03 – – 4.19 7.74 5.07 2.22 2.38 3.54

RIV was calculated as the mean of relative cover and relative frequency. Only RIV > 2.0 are shown.

separation of the six stand age/aspect categories, indicating strong compositional variation relative to age and topographic position. Herb layer composition along CCA axis 1 (l = 0.485) was positively correlated with slope aspect (r = 0.805) and soil organic matter content (greater on NE aspects; r = 0.562) and negatively correlated with soil C/N ratio (greater on SW aspects; r =
0.606; Fig. 4A). Axis 2 represented a weaker gradient (l = 0.164), generally separating clearcut versus mature forest quadrats, with greater spring light availability (r = 0.532) and air temperatures (temperature; r = 0.511) in clearcut quadrats. CCA ordination of summer herb communities showed similar but slightly weaker vegetation–site relationships (Fig. 4B). Slope aspect (r =
0.766), soil organic content (greater on NE aspects; r =
0.491), and C/N ratio (greater on SW aspects; r = 0.449) again were strongly correlated with herb composition along axis 1 (l = 0.389); temperature (r = 0.408) and summer light availability

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(r = 0.294) showed significant but weaker correlations (SW aspects). Variables correlated with herb layer composition along axis 2 (l = 0.181) were summer light availability (r = 0.328), with greatest intensities in mature forest quadrats, and sapling cover (r =
0.672) and temperature (r =
0.260), increasing in clearcut quadrats. Most variables selected for final CCA analyses showed significant pair-wise correlations with other measured environmental variables (Table 2). Topographic aspect, used to represent a complex gradient of edaphic and other microenvironmental variables in this study, showed significant Spearman-rank correlations with soil C/N (r =
0.54), Mg (r = 0.47), N (r = 0.41), and organic matter (r = 0.47; each P < 0.001). Other particularly strong correlations were found between soil organic content and Mg (r = 0.76), Ca (r = 0.69), and moisture (r = 0.58; each P < 0.001). Soil C/N ratio was negatively correlated with soil N (r =
0.59), Mg (r =
0.58), Ca (r =
0.46), moisture (r =
0.42), and organic content (r =
0.43; each P < 0.001). Sapling cover, important in the summer CCA ordination of herb layer data, exhibited strong negative correlations with tree basal area (r =
0.81) and leaf litter depth (r =
0.60; P < 0.001; Table 2). The relationship of understory species richness to soil C/N was best fit by linear regression models. Soil C/N ratio was a strong predictor of understory richness in spring forests (r2 = 0.634, P < 0.0001; Fig. 5), with higher herb richness at lower soil C/N. Spring clearcuts showed a significant but weaker relationship of richness and C/N (r2 = 0.309, P < 0.0001; Fig. 5), with a less negative regression slope (P < 0.001). These relationships varied with topographic aspect, with significant negative associations between richness and soil C/N in SW and INT forest quadrats and SW clearcut quadrats. SW quadrats tended to show less variability in herb richness, generally with fewer than 10 species per quadrat, and greater variability in C/N ratios than INT and especially NE aspects. Consequently, the slope of the richness versus C/N regression line was steeper and more negative for INT than for SW forest aspects (P < 0.001; Fig. 5). No relationship between soil C/N and richness was found for NE aspects (both stand ages) or INT clearcut quadrats, which showed very little variability in C/N (Fig. 5). For the summer sample period, similar but

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Fig. 4. Canonical correspondence analysis ordinations of 192–2.5 m2 herb quadrats for spring (A) and summer (B) sample periods. Vectors represent the strength and direction of correlation between species composition and environmental variables. Note lower x and left y-axes (
3 to 3 range) used for quadrat scores and upper x and right y-axes (
1 to 1 range) used for environmental variable scores. Aspect = topographic aspect; C/N = soil C/N ratio; organic = soil organic content (%); sapling cover = mean cover of saplings (%) (woody stems < 2.5 cm DBH and >30 cm tall) per quadrat; spring light = spring open sky (%); summer light = summer open sky (%); temp = air temperature.

less pronounced negative regressions were obtained, again with a stronger relationship of richness to soil C/N in mature relative to young stands (r2 = 0.269 versus 0.134, respectively; each P < 0.0001; results not shown). Like richness, herbaceous cover declined with increasing soil C/N, particularly across mature forest quadrats (r2 = 0.492, P < 0.0001; Fig. 6). Clearcut quadrats showed a weaker relationship of cover to C/N

(r2 = 0.152, P < 0.001). Unlike richness, slopes of regression lines for young and mature forests did not differ significantly. The relationship of herbaceous cover to C/N ratio again varied with aspect position, with a steeper, more negative relationship of cover to C/N in INT than SW forest quadrats (P < 0.001; Fig. 6) and no relationship in NE samples. Slopes of clearcut regression lines did not differ with aspect position.

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Table 2 Pair-wise Spearman-rank correlation coefficients of measured environmental variables and variables selected for final CCA ordinations (column variables)

Aspect Soil moisture (%) Soil organic matter (%) Soil P (mg g
1) Soil K (mg g
1) Soil Ca (mg g
1) Soil Mg (mg g
1) Soil N (%) Soil C/N Soil compaction (MPa) Leaf litter depth (cm) Air temperature (8C) Spring light (%) Tree basal area (m2 ha
1) Tree density (stems ha
1) Sapling cover (%) Seedling cover (%)

Aspect

Organic matter

Temperature

Spring light

Sapling cover

C/N

1.00 0.35 0.47 0.39 0.27 0.38 0.47 0.41
0.54
0.19 0.03
0.10 0.03 0.25 0.27
0.18
0.49

0.47 0.58 1.00 0.40 0.46 0.69 0.76 0.43
0.43
0.01 0.03
0.12
0.08 0.09 0.17
0.04
0.33


0.10
0.02
0.12
0.02
0.02
0.05
0.06
0.24 0.30 0.42
0.49 1.00 0.39
0.54 0.47 0.53 0.25

0.03
0.11
0.08
0.13 0.04
0.02 0.00
0.02 0.18 0.28
0.56 0.39 1.00
0.40 0.31 0.48 0.21


0.18
0.04
0.04
0.05 0.00 0.13 0.02
0.13 0.33 0.41
0.60 0.53 0.48
0.81 0.47 1.00 0.24


0.54
0.42
0.43
0.22
0.39
0.46
0.58
0.59 1.00 0.31
0.07 0.30 0.18
0.39 0.16 0.33 0.37

Only variables with significant correlations (P < 0.001; bold), based on Bonferroni-adjusted probabilities, are shown.

4. Discussion The herbaceous layer at our study site was highly responsive to both forest management disturbance (stand age/clearcutting) and site conditions (e.g., topography, soil fertility, and C/N ratio), with generally greater richness and abundance of herbaceous species in younger stands and on more moist, fertile aspects and slope positions. Increases in herbaceous diversity following logging are consistent with Roberts and Gilliam (1995; on mesic sites) and Bormann and Likens (1979), who found greater richness in recently clearcut deciduous forest stands (25–75 years). During this stand initiation stage, stand dynamics and microenvironmental conditions exhibit greatest variability, changing more rapidly and dramatically than in any other stage of forest development (Bormann and Likens, 1979; Oliver and Larson, 1990). This increased spatial heterogeneity and resource availability has been linked to such increased diversity (White and Pickett, 1985; Oliver and Larson, 1990). In both spring and summer samples, we found lower soil N and higher C/N ratios in the A-horizon of these recently logged stands. Bormann and Likens (1979) found removal of the forest canopy to increase soil temperatures and moisture, thereby increasing

organic matter decomposition and N mineralization, resulting in net losses of C and N above those associated with biomass removal. Johnson (1995) found similar declines in forest floor C and N following clearcutting. Alternate explanations for losses of forest floor organic matter following harvesting have been proposed by Yanai et al. (2003). This nitrate leaching appears to vary seasonally and with stand age and site fertility (Wiklander, 1981). Demand for N generally peaks just before canopy closure in vigorously growing, aggrading forests (e.g., revegetating clearcuts), as competition for light, soil resources, and growing space reaches its maximum (Miller, 1981; Oliver and Larson, 1990; Fenn et al., 1998). We found higher levels of soil N in mature second-growth stands, those in the understory reinitiation stage, likely due to less vigorous growth and reduced stem density (Small and McCarthy, 2002). Greater importance of leguminous species (D. glutinosum and A. bracteata), important N-fixers in terrestrial ecosystems, may have further enhanced soil N levels on these sites (Vitousek et al., 2002). While herb layer composition and diversity varied significantly with stand age at our study site, topographic and edaphic features showed the most pronounced influence on understory dynamics. Such

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Fig. 5. Simple linear regression of spring mean herb richness on soil C/N ratio in 2.5 m2 sample quadrats in mature forest stands (n = 96) and revegetating clearcut stands (n = 96). SW = southwest-, INT = northwest- and southeast-, and NE = northeast-facing slopes, respectively.

site variability is likely to be an important determinant of understory disturbance response (Collins et al., 1985; Meier et al., 1995; Roberts and Gilliam, 1995). Like Hutchinson et al. (1999) in second-growth oak forests of southern Ohio and Huebner et al. (1995) in a beech-maple forest of southern Indiana, we found greater herb layer richness and cover on more mesic aspects and slope positions. These aspect influences have been widely recognized in the central Appalachians and other

north-temperate areas of moderate to high relief, where south-facing slopes generally experience higher temperatures and light intensities and lower moisture and fertility than north-facing slopes (Cantlon, 1953). These microclimatic differences are often greatest just above ground level, exerting particularly strong influence on understory vegetation (Cantlon, 1953; Small and McCarthy, 2003). In our study, the greater abundance and diversity of herb layer species on mesic sites corresponded to

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Fig. 6. Simple linear regression of spring mean herb abundance (% cover) on soil C/N ratio in 2.5 m2 sample quadrats in mature forest stands (n = 96) and revegetating clearcut stands (n = 96). SW = southwest-, INT = northwest- and southeast-, and NE = northeast-facing slopes, respectively.

higher soil N and lower C/N ratios. Composition of the herbaceous layer was also strongly correlated with soil C/N throughout the growing season. Low C/N ratios have been associated with increased substrate quality, particularly for microbial N utilization (Paul and Clark, 1989). Soil C/N ratios comparable to those at our study site (mean C/N 15.35  0.20) have been linked to net N mineralization (Paul and Clark, 1989) and, at the regional scale,

with increased nitrate concentrations in surface waters (Helliwell et al., 2001). It is important to note that data on soil C, N, and C/N at our study site were collected during the 2000 growing season, whereas vegetation and other edaphic and environmental parameters were measured in 1998. Similar vegetation–environmental relationships and trends in soil fertility for the 1998 data alone (based on different measured parameters) support the 1998/2000

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correlations, as both revegetating clearcut and mature forest samples showed greater fertility on NE versus SW aspect positions (higher Ca, Mg, Ca:Al, organic matter) and compositional variations with site quality in 1998 (Small and McCarthy, 2002, present study). However, as forest understory vegetation and edaphic variables may show considerable year-to-year variation, such correlations must be interpreted cautiously. Broad-scale correlations of understory richness and composition with N availability have been found in other forests of the region (e.g., Hutchinson et al., 1999). However, even within a single forest type, as in our study, we observed considerable variation in soil C/N and understory dynamics. Within our sites, C and N availability declined and C/N ratios increased on more xeric (SW) sites. Similar trends of lower C and N and higher soil C/N have been shown for SW relative to NE aspects (mean A-horizon C = 1.41% versus 3.25%, N = 0.176% versus 0.251%, Franzmeier et al., 1969; C/N = 17.6–21.6 versus 13.3–14.3, Finney et al., 1962) and upper relative to lower slope positions (mean A-horizon C = 0.15% versus 1.98%, N = 0.20% versus 2.52%, Franzmeier et al., 1969) in other mixed oak forests of the northeast. We found the C/N of upper mineral soils to be a strong predictor of herbaceous abundance and richness, particularly on more N-limited (drier, less fertile SW slopes) mature forest sites. Greatest variability in soil C/N ratios was found on these sites, where herb layer characteristics were particularly responsive to C/ N. The weaker relationship of C/N to herb richness in younger stands (especially, INT and NE slopes) emphasizes the dynamic relationship of soil fertility and vegetation diversity through forest succession, perhaps due to decreasing light and increasing nutrient availability over time (Tilman, 1986). Interestingly, our conclusions differ from those of Gilliam et al. (1995) in a central Appalachian forest, who found allogenic factors, such as soil moisture and fertility, to be of greater importance in early succession and autogenic, stand characteristics to be of greater importance in later succession, based on stronger overstory–understory relationships in mature (relative to younger clearcut) stands. Differences in stand age and site-dependent factors may contribute to this apparent discrepancy. Tree density in our early successional clearcut stands (7 years; 3468 stems/ ha) well exceeded that of Gilliam et al. (20 years; 2099

stems/ha), resulting in severe summer light limitations. Gilliam (2002) and Whigham (2004) emphasize the negative influences of tree density and corresponding light limitations to plant growth in the herbaceous layer. Less limiting understory light environments in our mature stands (lower tree density and higher summer light availability) may have allowed greater response to edaphic variations. While most temperate deciduous forests remain N limited, high rates of N deposition in a number of central Appalachian forests (e.g., 15–20 kg ha
1 year
1 at Fernow, West Virginia, measured in 1992– 1993; Gilliam et al., 1996; Peterjohn et al., 1996) make the potential for N saturation particularly high (Stoddard, 1994; Fenn et al., 1998). In addition, some factors may ‘‘predispose’’ forests to saturation. In a review of several N saturated forests in eastern North America, Fenn et al. (1998) found greater stand age, reduced vigor, steep topography, and lower C/N ratios among the factors most important in explaining lower N retention capacities in saturated systems. Associated changes in soil N dynamics could undoubtedly affect forest dynamics and successional patterns. On the other hand, it has been suggested that excess N and associated ecological effects on nutrient-poor sites can lead to particularly dramatic changes in vegetation composition and diversity (Bobbink et al., 1998; Fenn et al., 1998). Understory composition at our study site was strongly correlated with variations in soil C/N, suggesting the potential for compositional shifts towards the mesic end of our gradient. Adkinson and Gleeson (2004) emphasize the importance of soil resources to understory productivity, with increased plant biomass (hence increased competition and reduced light availability) on more productive sites. Repeated fertilization treatments have produced similar increases in canopy cover, causing severe shading and reduced richness and abundance of understory herbs (Tamm, 1991). In oak forests of southern Sweden, increased N deposition has been correlated with greater frequencies of fast growing, nitrophilous or mesophytic understory species (Tyler, 1987). Bobbink et al. (1998) found similar increases in nitrophilous species across a wide range of aquatic and terrestrial systems experiencing increased N deposition. These N-demanding species may competitively exclude more typical understory herbs, those adapted to N-poor conditions, lowering overall species

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richness (Tilman, 1997; Bobbink et al., 1998). Nitrogen-fixing herbs, in particular, may be less competitive in habitats with excess N, diminishing in favor of more mesophytic species (Vitousek et al., 2002). At our study site, more fertile clearcut quadrats contained higher frequencies of non-native spring herbs (NE = 38% and INT = 27% versus SW = 6%) and woody seedlings (NE = 35% and INT = 29% versus SW = 0%), suggesting that N additions may also encourage the spread of introduced species into deciduous forest understories. Whereas the herbaceous layer represents only a tiny fraction of above-ground living biomass and net primary production in temperate deciduous forests (Muller, 2003), repeated use of this stratum as an indicator of forest health, integrity, and site conditions (e.g., Pregitzer and Barnes, 1982; Meilleur et al., 1992) emphasizes its critical role in the dynamics of these systems. In particular, ephemeral spring herbs, in conjunction with soil microbes, appear to play a vital role in controlling nutrient losses during periods of high N mineralization (spring snowmelt, i.e., a vernal dam; Muller and Bormann, 1976; Zak et al., 1990). The spring flora may subsequently serve as a source of nutrient additions through deposition of rapidly decomposing litter (Muller, 2003). In this study, the strong correlations between soil N levels and herb layer composition, abundance, and diversity emphasize the influence of soil N on herbaceous layer dynamics in both young and mature stands and especially more nutrient-poor (SW) sites. However, as demonstrated by Eickmeier and Schussler (1993), significant increases in N and P sequestration by the spring ephemeral Claytonia virginica in response to experimental nutrient increases emphasize the potential for the ‘‘vernal dam’’ to not only control nutrient levels but to respond to changes in soil N availability (also Anderson, 2003). Conversely, studies in opposition to the vernal dam concept (e.g., Jandl et al., 1997) suggest that an abundance of spring herbs on more productive sites could actually increase nutrient leaching, with decomposition of N-rich herbaceous foliage enhancing microbial activity and overall rates of litter decomposition. While our study does not allow us to isolate causal factors (N availability versus herbaceous retention of nutrients), the tight relationship of soil N and particularly C/N ratios to herb layer dynamics

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suggests that changes in soil N with atmospheric N deposition could critically affect understory community dynamics. Influences of elevated N deposition on eastern forests should be expected to be site-specific, varying even within relatively uniform forest types, such as ours, with potentially greater influence on more nutrient-poor sites and maturing forests (those approaching a steady state; Bormann and Likens, 1979). Since herb layer interactions not only influence nutrient retention and losses from forested systems but also are tightly linked (through competitive interactions) to the success of woody species in reaching the forest canopy (Wilson and Shure, 1993; George and Bazzaz, 1999), such changes in understory dynamics have the potential to significantly influence overstory recruitment patterns, stand structure, and broader ecosystem responses to N deposition.

Acknowledgements We gratefully acknowledge the Ohio Biological Survey, the John Houk Memorial Research Fund, and the Department of Environmental and Plant Biology at Ohio University for financial support, the Waterloo Wildlife Experiment Station, Ohio Department of Natural Resources, for permission to conduct this study, and D.C. White and R.G. Verb for field assistance.

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