Forest Ecology and Management 258 (2009) 2556–2568

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Forest Ecology and Management

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Patterns of plant community structure within and among primary and second-growth northern hardwood forest stands

Julia I. Burton a,*, Eric K. Zenner b, Lee E. Frelich c, Meredith W. Cornett d a Department of Forest and Wildlife Ecology, University of Wisconsin – Madison, 1630 Linden Drive, Madison, WI 53706, United States b School of Forest Resources, The Pennsylvania State University, 305 Forest Resources Building, University Park, PA 16802, United States c Department of Forest Resources, University of Minnesota, 115 Green Hall, 1530 Cleveland Avenue North, St. Paul, MN 55108, United States d The Nature Conservancy in Minnesota, 394 Lake Avenue South, Duluth, MN 55802, United States

ARTICLE INFO ABSTRACT

Article history: Forest scientists advocate the use of natural disturbance-based forest management for restoring the Received 4 May 2009 characteristics of old-growth forests to younger second-growth northern hardwood stands. However, Received in revised form 4 August 2009 prescriptions rely upon studies that have (1) not spanned the full range of conditions and species Accepted 5 September 2009 assemblages, and (2) focused primarily on contrasting old-growth and mature second-growth stands at a single scale. To examine how the legacy of historical logging activities influences forest structure and Keywords: function, we compared and contrasted patterns of plant community structure within and among second- Forest structure growth and primary stands on the north shore of Lake Superior in Minnesota, USA — near the current Natural disturbance-based forest range limits of the dominant species, sugar maple (Acer saccharum). We expected second-growth stands management Old growth to be in younger developmental stages, and structurally less heterogeneous both within and among Primary forest stands. Furthermore, we expected those differences to be associated with patterns of plant community Second-growth forest composition and diversity. Understory vegetation Three of the four primary stands and one of the eight second-growth stands were in the old-growth stage of development. Yellow birch (Betula alleghaniensis) and conifers as a group (Thuja occidentalis, Picea glauca and Abies balsamea) were more abundant, and yellow birch was more variable, within primary stands than second-growth stands. The volume and heterogeneity of coarse woody debris in intermediate decay- and size classes was also greater within and among primary stands relative to second-growth stands. While mean subplot richness of overstory tree species was greater in primary stands, mean quadrat richness, and rates of species accumulation for forest herbs as well as total herbaceous cover, and graminoid cover were greater in second-growth stands. Furthermore, total basal area (BA), the BA of conifer species, the density of yellow birch trees, understory vegetation and light transmittance were more variable among second-growth stands. At the multivariate level, primary stands were distinguished from second-growth stands not by differences in stand structure, but by a greater abundance of yellow birch and conifer species in the canopy, which was also related to O-horizon depth and understory plant species composition and structure. Differences in community structure between primary and second-growth stands may have resulted from the original cutover as well as high- grade logging, which together may have disrupted the mechanisms that maintain populations of important co-dominant tree species and associated understory plant communities in northern hardwood stands. ß 2009 Elsevier B.V. All rights reserved.

1. Introduction natural disturbance, historical landscape and stand structures, and historical ranges of variation (Attiwill, 1994; Franklin et al., 2002; The potential degradation of forest ecosystem goods and Seymour et al., 2002; Drever et al., 2006). For northern hardwood services and loss of biodiversity due to extensive logging has forests, specific efforts include those that attempt to accelerate generated an impetus for developing silvicultural systems that succession in younger second-growth stands by imposing the sustain biodiversity and productivity by mimicking patterns of structures that characterize historical landscapes and old-growth stands (Lorimer and Frelich, 1994; Keeton, 2006). However, previous studies have focused primarily on average conditions * Corresponding author. Tel.: +1 608 265 6321; fax: +1 608 262 9922. or a single scale and have not included stands near the range limits E-mail address: [email protected] (J.I. Burton). of north-temperate tree species; thus, the legacy of historical

0378-1127/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2009.09.012 J.I. Burton et al. / Forest Ecology and Management 258 (2009) 2556–2568 2557 logging events on the composition, structure and function of light transmittance and understory plant communities, which are second-growth stands is not fully understood. Because interactions more fine-grained and patchy in old-growth stands (Crow et al., among structure, composition and variability at multiple scales 2002; Scheller and Mladenoff, 2002). Although Duffy and Meier may be important for maintaining the resilience of northern (1992) report devastating effects of logging on the richness and hardwood forest ecosystems, restoration strategies based solely on cover of forest herbs in the southern Appalachians, evidence from average conditions and successional processes may serve only to the Lake States suggests that timber harvesting may increase reinforce current differences between primary stands that were herbaceous species richness and cover due to the immigration of never logged and second-growth stands. weedy and non-native species (Metzger and Schultz, 1984; Most of the northern hardwood forests in the upper Great Lakes Scheller and Mladenoff, 2002). region regenerated after extensive logging, known as the cutover, Here we investigate differences in community structure and that occurred at the turn of the 20th century (Zon, 1925). Logging heterogeneity between primary forests with a history of natural at this time ranged from the selective removal of economically disturbance and regeneration, and second-growth forests that valuable tree species to heavy partial cuts and clear-cutting were logged during the cutover and subsequently high-graded in oftentimes followed by repeated uncontrolled slash fires (Stearns, northeastern Minnesota. We expected second-growth stands to be 1997). This series of events in particular reduced the area of in younger developmental stages, and structurally less hetero- unharvested, primary stands and stands in the old-growth stage of geneous both within and among stands. Furthermore, we expected development in Minnesota to 0.2% and 2% of the pre-Euro- those differences to be associated with patterns of diversity and American extent, respectively (Frelich, 1995). plant community composition and structure. By comparing and While the cutover greatly reduced the extent of old growth on contrasting primary and second-growth stands with respect to the landscape, it may have also initiated more persistent changes structure, species composition and diversity at multiple scales, we in community structure in regenerating second-growth stands. In can characterize the persistent effects of natural and anthropo- northern hardwoods of the upper Great Lakes region, the natural genic disturbance regimes to inform guidelines for managing and disturbance regime resulted in a shifting mosaic of stands in restoring structure and composition to second-growth stands. different stages of development dominated by old growth (Frelich and Lorimer, 1991). Within stands, the volume of coarse woody 2. Study area debris (CWD), snag basal area (BA), total area in gaps and average gap size increase in later stages of development (Tyrrell and Crow, Sugar maple-dominated northern hardwood forests are dis- 1994; Dahir and Lorimer, 1996). Studies from the Pacific North- tributed along the ridge tops on the north shore of Lake Superior west show that the range of structural variation and structural within the transition zone between north-temperate and south- heterogeneity indeed increases with stand age (Spies and Franklin, ern-boreal forests. Elevations range from 200 to 700 m and the 1988; Zenner, 2004). Furthermore, compared to conventional topography is gently rolling to steep. Lake Superior moderates the systems of forest harvesting, natural disturbances can also lead to climate, which is cold-temperate continental, with a mean more complex structures and greater residual heterogeneity growing season length of 104–168 frost-free days (base tempera- (Hanson and Lorimer, 2007). ture = 0 8C), mean annual temperature of 4.72 8C, and mean annual Heterogeneity of important community attributes can be both precipitation of 77.50 cm with 150.4 cm of snowfall (1971–2000, affected by disturbance, and influence the response of forests to Midwest Regional Climate Center, http://mcc.sws.uiuc.edu). disturbance (Fraterrigo and Rusak, 2008). In northern hardwood This study is part of the pre-treatment phase of a larger project forests, sugar maple trees can form dense layers of advance that examines methods of restoring the composition and structure regeneration that excludes light-seeded and mid-tolerant tree of primary stands to second-growth stands. Twelve northern species. Periodic moderate-severity disturbances that create large hardwood stands located in Lake County in northeastern canopy openings coincident with seedbeds of rotting CWD and tip- Minnesota were selected on the basis of cover type, logging up mounds may therefore be important for preventing competitive history and lack of recent major natural disturbance (Fig. 1, exclusion by permitting light-seeded tree species such as yellow Table 1). The selected primary and second-growth stands were birch and conifers in stands to regenerate and ascend to a canopy composed of a sugar maple-dominated overstory. Less abundant position (Connell, 1979; Cornett et al., 1997; Carlton and Bazzaz, overstory species included yellow birch, conifers such as northern 1998; Woods, 2004). Patterns of herbaceous vegetation are also white cedar (T. occidentalis), white spruce (P. glauca) and balsam fir associated with environmental heterogeneity imposed by canopy (A. balsamea), and other hardwood species including black ash openings (Moore and Vankat, 1986; Roberts and Gilliam, 1995), (Fraxinus nigra), paper birch (Betula papyrifera), northern red oak coarse woody debris (Scheller and Mladenoff, 2002) and the (Quercus rubra) and red maple (Acer rubrum). Four primary stands composition of the overstory (Beatty, 1984; Mladenoff, 1987; were located on state lands designated for the conservation and Canham et al., 1994; Barbier et al., 2008). Herbaceous vegetation preservation as old growth based on the presence of long-lived can interact with tree seedlings establishment after a disturbance species, lack of a recent catastrophic disturbance and little to no to influence micro-successional pathways (George and Bazzaz, direct human impacts (Rusterholz, 1996). Thus, stands managed 1999). Thus, spatial variability of key compositional and structural under the old-growth program in Minnesota were not necessarily attributes within forest stands can function to maintain popula- in the old-growth phase of development based on structural tions of some species over time and, ultimately, the diversity of the threshold definitions (e.g., Frelich and Lorimer, 1991; Frelich and system. Changes in community composition and/or a loss of Reich, 2003). The eight second-growth stands were located on structural heterogeneity may therefore degrade ecosystem resi- nearby county land. The greater sample size for second-growth lience, or the magnitude of disturbance that a system can stands reflects the design of the long-term experiment that experience before it shifts into an alternative state (Holling, 1973). examines the effects of two replicated (n = 4) structure manipula- Previous studies have documented that mature, second-growth tions on community structure and productivity, as well as the stands contain fewer large trees in the overstory and snags, and scarcity of primary stands in the study area. None of the stands lower coarse woody debris volumes (Goodburn and Lorimer, 1998, were selected based upon the selection of another stand. With the 1999; Hale et al., 1999; McGee et al., 1999) than old-growth stands. exception of two primary stands located within George Crosby- These structural differences between old-growth and mature, Manitou State Park (850 m apart), all stands are separated by second-growth stands are associated with divergent patterns in distinct physiographic and vegetation features or with a distance of 2558 J.I. Burton et al. / Forest Ecology and Management 258 (2009) 2556–2568

elevations (Table 1). Two of the primary stands were located in George Crosby-Manitou State Park, which was donated to the State of Minnesota to be preserved for primitive outdoor recreation. The other two primary stands are on smaller tracts, also owned and managed by the State of Minnesota as part of the old-growth conservation program (Rusterholz, 1996). Because of the lack of substantial physiographic variation between stands (Fig. 1, Table 1), primary stands provide a reasonable reference to which we can compare second-growth stands of logging origin (Frelich et al., 2005).

3. Methods

3.1. Field sampling

In each of the 12 stands, we established a 120 m 120 m (1.44 ha) research plot in the spring of 2003. Twenty-five circular Fig. 1. Locations of primary stands are indicated by circles, second-growth stands nested subplots for sampling the overstory, mid-story and ground- are triangles. Base layer is 30 m digital elevation model with hill shade. Inset shows study area location (star) within Minnesota (white) and the upper Great Lakes layer vegetation were established on a 30 m 30 m grid. A 30 m region. distance between subplot centers was chosen so the extent of sampling would exceed reported ranges of spatial dependence, and allow us to quantify the heterogeneity of important community at least 1 km. The two primary stands in the State Park were attributes (e.g., Scheller and Mladenoff, 2002). Ground-layer separated by other stages of development and would be vegetation was sampled twice during the growing season from considered different stands in management. Furthermore, dis- mid-May through mid-September, and diffuse light transmittance tances between stands did exceed reported ranges of spatial (%light) measurements were taken before leaf fall between dependence for the variables examined in this study. Therefore we September 6 and September 14, 2003. are comfortable considering the stands independent and not Overstory vegetation within a 10 m radius from the subplot pseudo-replicates (e.g., Hurlbert, 1984). centers was sampled in all 25 subplots in each of the 12 stands Although the details about the specific histories of each second- (with the exception of one second-growth stand (BH), which had a growth stand are unknown, county-managed lands were forfeited limited sample of 22 subplots). We recorded the species, condition due to tax delinquency after being logged between the late 1890s (i.e., live or dead snag), and diameter at 1.37 m (dbh) for all and the mid 1920s and burned subsequently in uncontrolled slash trees 10 cm dbh. For a sub-sample of 56 trees that were fires (Tikkanen et al., 1995). High-grading was widely criticized selected to represent a replicated sample of the range of existing because it resulted in residual stands that were dominated by diameters and species, we measured crown radii in four cardinal poor-quality timber of little merchantable value (Eyre, 1939); directions to estimate exposed crown area (ECA). ECA was however, it was also promoted specifically in northern hardwood calculated as the sum of four quarter ellipses for crown radii of stands in the Lake States as a means to provide critical lumber measured trees and estimated for other trees based on regressions grades for the war effort (Stott, 1943). Furthermore, many county of ECA on dbh (log(ECA) = 0.1446 + 0.1060dbh 0.0006dbh2, stands were selectively harvested for high-grade timber repeat- p < 0.001, r2 = 0.70). edly, and particularly for conifer species and yellow birch (Dan Tree saplings and shrubs 1 m tall but <10 cm dbh were tallied Spina and Chris Dunham, personal communication). by species within a 2 m radius of subplot centers. Percent cover of Land use history, such as logging, is oftentimes related to the ground-layer vegetation (<1 m tall) was estimated by species physical features such as topography and soil fertility. However, in within a 1 m2 circular quadrat directly once in the spring prior to this landscape, there do not appear to be any characteristics unique the senescence of spring ephemeral species and once in the to primary or second-growth stands. First, both primary and summer. The percent cover of leaf litter, rocks, CWD (5cm second-growth sites are distributed on similar soils at comparable diameter), exposed mineral soil (EMS) and mosses was estimated

Table 1 Developmental stage classes (old growth = OG) and physiographic characteristics of primary and second-growth stands.

Stand by type Stage Lat. Long. Elev. (m) Slope (%) Aspect (8) Area (ha) Light (%) Soil texture

Primary Caribou river (CR) OG 47.5082 91.0602 430 5 131 38.31 3.6 Loamy–very fine Egge pond (EP) Mature 47.4669 91.2276 553 4 75 71.40 3.1 Loamy–very fine Manitou north (MN) OG 47.4680 91.1137 463 8 214 36.06 1.4 Loamy–coarse loamy Manitou south (MS) OG 47.4603 91.1135 461 8 350 57.87 1.0 Loamy–coarse loamy

Second-growth Big pine (BP) Mature 47.4771 91.1496 465 8 162 40.47 1.8 Loamy–coarse loamy Birch cut (BC) OG 47.4500 91.1885 450 6 119 25.60 No data Loamy–very fine Brush hog (BH) Mature 47.4510 91.2041 479 1 157 16.54 11.6 Loamy–very fine Cedar finger (CF) Mature 47.4553 91.2037 478 1 83 16.54 1.9 Loamy–very fine East Egge (EE) Mature 47.4570 91.2130 515 1 226 22.05 1.6 Loamy–very fine Hill top (HT) Pole 47.4853 91.1354 489 8 273 13.78 No data Loamy–coarse loamy Power line (PL) Mature 47.9378 91.2037 390 10 142 19.67 No data Fine loamy–hemic Schoolhouse trail (ST) Pole 47.4592 91.1977 478 2 327 23.62 2.0 Loamy–very fine

Latitude (Lat.) and Longitude (Long.) are given in decimal degrees. Elevation (Elev.), slope and aspect were derived from a 30-m resolution digital elevation model. Light (%) was measured at 2 m using a Licor LAI 2000 at a subset of plots. Soil texture was derived from a soils map of Minnesota (Cummings and Grigal, 1981). J.I. Burton et al. / Forest Ecology and Management 258 (2009) 2556–2568 2559 for all quadrats as well. For all CWD 5 cm within the 10 m subplot BA were also calculated for statistical comparison of stand types for radius, we also measured the diameter at each end and the length sugar maple (SM), yellow birch (YB), conifers and other hard- in order to estimate volume. Decay classes (DC) were visually woods. determined based on the presence of foliage, the shape and CWD volume was calculated using the equation for a frustum of integrity of the wood, where: DC1 = recent, DC2 = solid, DC3 = so- a cone (Harmon and Sexton, 1996; McGee et al., 1999) and lid-decayed, DC4 = decayed and DC5 = very decayed (Tyrrell and summed for each decay and size class. Size classes were based on Crow, 1994). Depth of the organic horizon (O-horizon) was the diameter at the mid-point of the log. Size classes were measured once in the center of each of four quadrants of each consistent with the diameter classes used for the classification of quadrat during the summer sample by piercing the forest floor overstory trees described above. with a ruler until encountering mineral soil. To maximize The density of saplings and shrubs 1 m tall and <10 cm dbh consistency, all quadrats were sampled by Burton. Additionally, was scaled up to a per hectare basis, and percent cover of woody to measure the weight of the O-horizon, we collected all leaf litter vegetation <1 m tall was calculated for each of the following and non-woody organic matter within a 0.10 m2 frame placed on groups: sugar maple, yellow birch, conifers, other hardwoods and the forest floor at a random distance between 1 and 5 m north of shrubs. To analyze the ground-layer vegetation, we combined each quadrat. The samples were air-dried until arrival at the lab spring and summer data. When species were observed in both where they could be oven-dried at 50 8C to a constant weight sampling periods, we used the larger cover estimate for analyses. within 1 g. For herbaceous species, we calculated total cover (all herbaceous Diffuse light transmittance (%light) was measured at 1 m and species combined), as well as the cover of the following guilds of approximately 2 m above the subplot centers in five second- herbs: ferns, fern allies, graminoids (species in the Poaceae, growth stands and all four primary stands using the LAI-2000 plant Cyperaceae and Juncaceae families), spring ephemerals, early- canopy analyzer (LI-COR, Lincoln, Nebraska). The LAI-2000 summer forbs, late-summer forbs and vines. Spring ephemerals (SE measures the integrated gap fraction at five concentric angles forbs) are defined as forbs that emerge and senesce prior to canopy simultaneously (Welles and Norman, 1991). Open-canopy mea- closure, early-summer forbs (ES forbs) emerge early in the spring surements were taken concurrently from either a nearby clear-cut and persist through canopy closure, reaching peak coverage before or from the middle of a lake in a canoe, depending on which type of midsummer, and late-summer forbs (LS forbs) reach peak coverage opening was nearest to the plot. Below-canopy measurements after midsummer (Givnish, 1987). were matched with the closest-in-time above-canopy measure- To examine patterns of diversity, we calculated mean subplot ments and %light was calculated using the post-processing species richness (quadrat/subplot richness) and total species software C2000 (LI-COR, Lincoln, Nebraska). All measurements richness per plot (plot richness) for all species and strata combined, were taken either under cloudy or overcast sky conditions, in the as well as for life forms (i.e., trees, shrubs and herbs) and strata (i.e., morning before sunrise or at dusk. overstory, mid-story and ground layer) separately. Average herbaceous species richness for all possible combinations of 1– 3.2. Characterization of community structure 25 subplots (m2) for each plot was calculated in PC-ORD (McCune and Mefford, 1999) for a comparison of species-area curves. We assigned each stand to one of four developmental stages: In addition to calculating the averages of the attributes pole, mature, old-growth, and mature-sapling mosaic (Table 1). described above to characterize the average structural and The classification system was developed in a set of 70 primary compositional conditions at the stand scale, we calculated northern hardwood stands located in Michigan’s Upper Peninsula standard deviation and range of all subplot values for each plot (Frelich and Lorimer, 1991). Assignments were based on the to quantify within-stand heterogeneity and the range of variation. aggregate exposed crown area (ECA) in the pole (10–24.9 cm dbh), These metrics provide a means to measure absolute levels of mature (25–44.9 cm dbh), and large (45 cm dbh) size classes variability in the same units as the data that can be compared using (Helms, 1998). Stands were classified as (1) old growth when 67% standard univariate statistics (Fraterrigo and Rusak, 2008). of ECA was occupied by large and mature trees with more crown Among-stand (landscape-scale) variability (dispersion) was quan- area in large than mature trees; (2) mature 67% of ECA was tified for the mean, standard deviation and range of each attribute occupied by large and mature trees with more crown area in by calculating the absolute deviations of each stand from the mean mature than large trees or when 67% ECA was occupied by poles value of its associated group (i.e., primary or second-growth). and mature trees with more crown area in mature trees than poles; (3) pole when 67% ECA was occupied by poles and mature trees 3.3. Statistical analysis with more crown area in poles than mature trees; and (4) mature- sapling mosaic when a stand did not meet any of the criteria We used t-tests to investigate differences in stand averages and described above. Stand classifications were derived from aggre- variability measures (i.e., standard deviations and ranges calcu- gated subplot data. lated from sub-samples) of compositional and structural commu- To examine differences in structural attributes among primary nity attributes between primary and second-growth stands. and second-growth stands, we calculated basal area (BA, m2 ha1) Levene’s test (Levene, 1960) was used to evaluate the assumption and live tree density (TPH, trees ha1) as well as metrics derived of equal variances (Schultz, 1985), which were pooled when from the distribution of total ECA including the 5 cm diameter class differences were not statistically significant (a = 0.10). When with the greatest aggregate ECA (Modal D) and the percentage of variances were not equal, Satterthwaite’s approximation of aggregate ECA in large trees (%large, trees 45 cm dbh). Structural standard errors was used for the tests (Zar, 1974). Levene’s test attributes based on the distribution of total ECA among size classes for equal variances was also used to examine differences in the of trees have been used to distinguish forest developmental stages dispersion of community attributes among primary and secondary more accurately than stem density or quadratic mean diameter, stands (Fraterrigo and Rusak, 2008). To compare herbaceous and may therefore be more useful than conventional metrics for species-area curves between primary and second-growth stands, describing the structure of the live overstory (Lorimer and Frelich, we used a mixed effects model. Species richness and area (i.e., the 1998; Goodburn and Lorimer, 1999) and relating forest structure to number of subplots) were log transformed prior to analysis other attributes quantitatively. Structural attributes were calcu- (Arrhenius, 1921) and species-area relationships were nested in lated for each subplot for all species combined. Density (TPH) and the random effect (i.e., plot). Because of the limited sample size of 2560 J.I. Burton et al. / Forest Ecology and Management 258 (2009) 2556–2568 primary and second-growth stands in this study, statistical tests deviations and ranges of YB BA (p = 0.005 and 0.028, respectively) were expected to have a low explanatory power and an increased and YB TPH (p = 0.007 and 0.064, respectively) were greater within probability of accepting the null hypothesis when the null primary stands than second-growth stands. On the other hand, hypothesis is false (type two error). To account for this effect mean SM BA (p = 0.013), conifer BA (p = 0.032) and the range of YB we chose an a-level of 0.10 for interpreting statistical significance TPH (p = 0.086) were more variable among second-growth stands (Neyman and Pearson, 1933) and interpreted p-values of 0.05–0.10 than primary stands (Table 4). as suggestive evidence for significant differences. All univariate analyses were performed in SAS for Windows (Version 9.1, SAS 4.2. Coarse woody debris and snags Institute 2006). Multivariate similarity between primary and second-growth The primary and second-growth stands exhibited differences in stands was compared using two non-metric multi-dimensional the distribution of CWD among decay and size classes. The average scaling (NMS) ordinations of (1) all compositional and structural volume of coarse woody debris in DC2 was greater in primary community attributes described above and (2) understory plant stands (p = 0.003), and was more variable within primary stands species in PC-ORD (McCune and Mefford, 1999). NMS avoids the than second-growth stands for standard deviations (p = 0.028) and assumption of linear relationships among variables and uses rank ranges (p = 0.085; Table 3). The volume of CWD in DC5 was more distances, linearizing the relationships between species abun- variable among primary stands than second-growth stands for dance and environmental variables (McCune and Grace, 2002). stand averages, standard deviations and ranges (p = 0.014, <0.001 NMS has been shown to perform better than other common and 0.002, respectively; Table 4). However, the range of mature ordination techniques for a range of data structures common to snags was more variable among second-growth stands (p = 0.044; community data (Minchin, 1987). It is an iterative approach that is Table 4). used more frequently today than historically due to increases in computing power. Structural and compositional attributes were 4.3. Understory vegetation and abiotic characteristics relativized across plots using a general relativization by column totals to eliminate differences in variable units, which could have The composition and structure of the understory varied caused some factors to influence the ordination disproportionately substantially between primary and second-growth stands at the (McCune and Grace, 2002). Rare species occurring in fewer than stand, within-stand and among-stand scales (Tables 3 and 4). At two plots were excluded from the second ordination of understory the stand scale, total herb cover and graminoid cover was greater species. We interpret axes by examining Pearson correlations in second-growth stands (p = 0.001 and 0.044, respectively; between the main matrix and plot ordination axis scores, and used Table 3). Within stands, graminoid cover was also more hetero- a nonparametric test to evaluate multivariate group differences geneous within second-growth stands, as shown by greater between primary and second-growth stands (multi-response standard deviations (p = 0.008) as well as ranges (p = 0.010). The permutation procedure, MRPP; Zimmerman et al., 1985). A among-stand variability of understory attributes was generally correlation of r > 0.58 is significant at an alpha = 0.05, a correlation lower for primary stands relative to second-growth stands of r > 0.50 is significant at an alpha = 0.10; therefore, we do not (Table 4). Average shrub density (p = 0.050), and the mean sapling report correlations lower than 0.50. Associations between plot axis densities, standard deviations and ranges were all more variable scores and %light were examined separately for the subset of plots among second-growth stands than primary stands for SM for which we did have %light data (Table 1). Both ordinations and (p = 0.001, <0.001 and 0.024, respectively) and conifers MRPP analysis used the Sørenson measure of similarity (Kruskal, (p = 0.061, 0.009 and 0.017, respectively). Furthermore, the 1964; Mather, 1976). average (p = 0.003), standard deviation (p = 0.015) and range of Finally, differences in the frequency and abundance of graminoid cover (p = 0.021), average late-summer forb cover individual herbaceous species between stand types were exam- (p = 0.047), the standard deviation and range of ground-layer ined using indicator species analysis (Dufreˆne and Legendre, 1997) shrub cover (p = 0.034 and 0.007, respectively), and the mean, in PC-ORD (McCune and Mefford, 1999). Statistical significance of standard deviation and range of both spring ephemeral (p = 0.043, indicator species was evaluated using 1000 Monte Carlo rando- 0.038 and 0.063, respectively) and early-summer forb cover mizations (McCune and Grace, 2002). (p = 0.037, 0.021 and 0.013, respectively) were greater among second-growth stands relative to primary stands. 4. Results Few corresponding differences in abiotic quadrat character- istics were observed at any scale, however. While O-horizon depth 4.1. Overstory composition and structure was more variable within (p = 0.059 and 0.049, respectively for standard deviations and ranges) and among (p = 0.057 for means) Three of the four primary stands were classified as old growth primary stands than second-growth stands, variability in the and the remaining one was mature. Of the eight second-growth standard deviation (p = 0.078) and range (p = 0.070) of diffuse light stands, one was classified as old growth, five as mature and two as transmittance (%light) at 2 m was greater among second-growth pole. Differences between primary and second-growth stands stands. depended upon the attribute as well as the scale at which it was examined (Table 3). Within stands, the range of modal diameters 4.4. Diversity (Modal D) was significantly greater within primary stands than second-growth stands (71.25 vs. 55.63 cm, p = 0.044). The For all taxa and strata combined, subplot richness was higher in standard deviation and range of BA within stands was more second-growth stands than primary stands containing 2.5 addi- variable among primary stands than second-growth stands tional species per subplot on average (p = 0.072, Table 2). Except (p = 0.003, Table 4) while average BA (p = 0.087) was more variable for cow parsnip (Heracleum lanatum) and hemp nettle (Galeopsis among second-growth stands. No other attribute describing the tetrahit), which were observed once each in a second-growth stand structure of the live canopy varied between stand types when and a primary stand, respectively, none of the species observed calculated for all species combined. However, average YB BA were exotic or considered weedy or otherwise invasive. Thus, this (p = 0.047), YB TPH (p = 0.066) and conifer BA (p = 0.015) were all difference could be explained by differences in native quadrat greater in primary stands (Table 3). Furthermore, the standard richness for herbaceous species. On average, second-growth J.I. Burton et al. / Forest Ecology and Management 258 (2009) 2556–2568 2561

Table 2 Subplot and plot scale species richness by guild and strata (SE in parentheses).

Subplot richness Plot richness

Primary (n = 4) Second-growth (n =8) T Pr > jtj Primary (n = 4) Second-growth (n =8) T Pr> jtj

All taxa and strata 7.82 (0.31) 10.32 (1.17) 2.07 0.072 39.75 (3.38) 48.75 (4.57) 1.29 0.227 Tree species (all strata) 2.73 (0.05) 2.37 (0.27) 1.33 0.222 8.75 (0.63) 8.00 (0.46) 0.95 0.366 Overstory trees 2.50 (0.08) 1.96 (0.22) 2.31 0.047 7.50 (0.65) 6.62 (0.32) 1.37 0.200 Tree saplings 1.08 (0.03) 1.11 (0.06) 0.37 0.721 2.75 (0.48) 2.88 (0.67) 0.15 0.882 Tree seedlings 1.19 (0.06) 1.43 (0.10) 1.60 0.073 4.50 (0.87) 4.63 (0.46) 0.14 0.891 Shrub species 0.86 (0.12) 1.13 (0.22) 0.83 0.427 5.00 (0.91) 7.25 (1.06) 1.36 0.205 Herbaceous species 4.23 (0.26) 6.83 (0.79) 3.13 0.013 26.00 (2.12) 33.50 (3.62) 1.38 0.197

accumulation (F = 51.91, p < 0.0001 for interactions between stand type and area). Differences in species-area curves became negligible at greater extents (Fig. 2). In contrast to herbaceous species, subplot richness of overstory tree species was lower in second-growth stands (p = 0.047). Yet, tree seedling quadrat richness was marginally greater in second-growth stands than primary stands (p = 0.073) (Table 2).

4.5. Multivariate associations between community attributes and stand origin

The final two-dimensional NMS ordination of community attributes (Table 3) captured 83.9% of the total variation in structural and compositional characteristics (58.3% of the variation on axis 1 and 25.6% on axis 2; Fig. 3), had a final stress of 11.56 and demonstrated greater structure than expected by chance (based on a Monte Carlo procedure, a = 0.05). Axis 2 corresponds most strongly to stand type, which is supported by differences in Fig. 2. Predicted species-area curves for primary (solid) and second-growth (dashed) stands. Points are observed means with error bars showing 95% confidence community structure between the stand types (MRPP; p = 0.024). intervals. For this mixed effects model, the effects of stand type (F = 5.65, p = 0.039) Furthermore, MRPP showed that the average multivariate distance and log(area) (F = 9715.75, p < 0.0001) and the interaction between them between second-growth stands (0.41) was greater than primary (F = 51.91, p < 0.0001) were significant. The random effect is not shown. stands (0.28). Overstory characteristics indicating a stronger co-dominance of contained 1.61 times the number of herbaceous species per square yellow birch and conifers in the overstory were strongly correlated meter in primary stands, a difference of 2.6 species per quadrat on with axis 2 and the locations of primary stands (r = 0.81, 0.73, 0.71 average (p = 0.013). Furthermore, species-area curves differed and 0.71 for conifer BA, YB TPH, conifer TPH and YB BA, between primary stands and second-growth stands (Fig. 2). respectively). Furthermore, the cover of YB seedlings was Primary stands contained fewer species, particularly within small positively associated with axis 2 (r = 0.56). In contrast, the cover areas, while second-growth stands had a greater rate of species of other hardwood seedlings (r = 0.81), spring ephemerals

Fig. 3. Non-metric multi-dimensional scaling ordination of primary and second-growth stands using stand averages of all community attributes (left) and understory species abundances (right). The main matrix variables structuring the ordinations and the percentage of variation in the data explained are given for each axis. Circles are primary stands and triangles are second-growth stands. Biplot overlays show the strength and direction of the correlations between community attributes and axis scores. All correlations with r2 0.50 (left) and r2 0.30 (right) are shown. BA, basal area; TPH, tree ha1; YB, yellow birch; SM, sugar maple; Con., conifer; Other, other hardwood species; %shrub, %cover of shrubs <1 m tall; O-H, O-horizon; ES, early summer; SE, spring ephemeral; CWD DC5, coarse woody debris in decay class five. 2562 Table 3 Comparison of community attributes between primary and second-growth stands at stand (mean) and within-stand scales (standard deviation and ranges).

Stand scale (mean of subplots) Within-stand heterogeneity (standard deviation of subplots) Range of variation within stands (range of subplots)

Primary (n = 4) Second-growth (n =8) T Pr > jtj Primary (n = 4) Second-growth (n =8) T Pr > jtj Primary (n = 4) Second-growth (n =8) T Pr > jtj

All tree species Modal D 49.70 (4.44) 42.79 (2.40) 1.51 0.162 17.20 (2.29) 15.65 (0.97) 0.74 0.475 71.25 (6.25) 55.63 (3.83) 2.25 0.049 %Large 33.34 (5.48) 25.16 (3.95) 1.20 0.257 22.46 (1.79) 22.65 (1.07) 0.10 0.926 73.16 (6.76) 70.05 (4.08) 0.42 0.686 2 1 BA (m ha ) 33.48 (0.87) 29.98 (1.48) 0.58 0.145 9.45 (1.41) 8.57 (0.48) 0.59 0.588 36.69 (5.56) 33.89 (2.69) 0.52 0.614 TPH (trees ha1 ) 563.41 (39.79) 597.85 (37.27) 0.57 0.580 174.43 (30.34) 169.98 (14.91) 0.15 0.883 676.41 (79.44) 704.42 (61.77) 0.27 0.795

Sugar maple BA (m2 ha1 ) 23.01 (0.45) 24.43 (2.50) 0.39 0.705 10.92 (1.09) 8.87 (0.49) 2.22 0.051 43.30 (6.00) 30.84 (2.40) 2.34 0.041 LTD (trees ha1 ) 469.57 (47.46) 519.69 (48.62) 0.65 0.531 206.96 (34.66) 188.97 (16.14) 0.55 0.597 859.44 (105.57) 708.24 (60.08) 1.35 0.208

Yellow birch BA (m2 ha1 ) 4.65 (1.13) 1.11 (0.31) 3.03 0.047 7.31 (1.19) 2.81 (0.67) 3.59 0.005 23.87 (3.14) 11.86 (2.87) 2.58 0.028 TPH (trees ha1 ) 26.42 (7.19) 6.60 (1.98) 2.66 0.066 36.78 (7.66) 13.83 (3.05) 3.38 0.007 127.32 (29.06) 47.75 (12.03) 2.53 0.064 2556–2568 (2009) 258 Management and Ecology Forest / al. et Burton J.I.

Conifers BA (m2 ha1 ) 4.55 (0.47) 1.90 (0.76) 2.94 0.015 6.44 (1.00) 3.67 (1.19) 1.50 0.164 25.45 (4.71) 14.51 (4.71) 1.45 0.179 TPH (trees ha1 ) 48.38 (7.85) 26.07 (12.82) 1.16 0.275 60.73 (9.43) 37.59 (15.14) 1.01 0.335 230.77 (47.53) 139.26 (55.44) 1.06 0.315

Other hardwoods BA (m2 ha1 ) 1.27 (0.64) 2.54 (0.76) 1.07 0.310 3.32 (1.28) 4.34 (0.87) 0.67 0.517 13.56 (4.66) 15.93 (2.69) 0.48 0.645 TPH (trees ha1 ) 19.10 (9.65) 45.49 (18.78) 0.94 0.368 39.23 (16.41) 71.06 (21.63) 0.96 0.361 143.24 (54.36) 258.63 (64.07) 1.16 0.274

Snag density Large (trees ha1 ) 11.14 (1.31) 8.28 (1.42) 1.28 0.230 18.21 (1.68) 16.32 (1.55) 0.75 0.469 55.70 (7.96) 51.73 (5.82) 0.40 0.699 Mature (trees ha1 ) 16.55 (3.16) 14.48 (1.92) 0.59 0.568 22.42 (2.89) 22.36 (2.42) 0.02 0.988 71.62 (7.96) 75.60 (11.94) 0.28 0.787 Pole (trees ha1 ) 31.19 (4.11) 35.81 (2.90) 0.92 0.394 35.11 (0.76) 38.48 (1.67) 1.36 0.203 151.19 (7.96) 135.28 (11.25) 1.25 0.239 Total (trees ha1 ) 58.89 (7.70) 58.57 (3.28) 0.05 0.965 44.80 (4.23) 42.45 (2.82) 0.47 0.647 167.11 (7.96) 163.13 (12.67) 0.21 0.849

Mid-story (stems ha1 ) Sugar maple 7504.10 (704.77) 9744.20 (2000.10) 0.76 0.320 6488.10 (792.64) 7988.50 (1401.9) 0.71 0.491 266.00 (2064.30) 30538 (5761.90) 0.62 0.413 Yellow birch 79.58 (45.94) 147.22 (83.12) 0.54 0.598 243.21 (140.89) 395.63 (214.25) 0.47 0.649 994.72 (596.83) 1591.50 (876.90) 0.45 0.664 Conifers 47.75 (9.19) 206.90 (98.11) 1.12 0.149 214.24 (37.57) 477.08 (196.79) 1.31 0.228 994.72 (198.94) 1890.00 (720.25) 1.20 0.265 Other hardwoods 15.92 (15.92) 55.70 (28.69) 0.93 0.376 79.58 (79.58) 254.03 (136.66) 0.85 0.415 397.89 (397.89) 1193.70 (672.55) 0.79 0.449 Shrubs 2251.39 (784.48) 3167.70 (958.02) 0.62 0.551 4003.70 (1168.10) 6524.90 (1908.60) 0.88 0.401 911.00 (5473.30) 28142.00 (8692.60) 0.93 0.373

Ground-layer woody (%cover) Sugar maple 42.67 (4.99) 33.62 (5.33) 1.08 0.307 29.63 (2.00) 24.68 (2.03) 1.53 0.157 91.00 (4.30) 81.5 (5.47) 1.13 0.286 Yellow birch 0.24 (0.08) 0.14 (0.05) 1.15 0.278 0.76 (0.26) 0.50 (0.17) 0.86 0.409 3.50 (1.19) 2.25 (0.75) 0.93 0.376 Conifers 0.29 (0.24) 1.14 (0.64) 0.90 0.390 1.39 (1.21) 3.78 (2.30) 0.70 0.501 6.75 (6.09) 17.13 (10.15) 0.68 0.512 Other hardwoods 0.92 (0.39) 1.96 (0.45) 1.46 0.174 3.37 (1.31) 3.99 (0.95) 0.38 0.713 16.75 (6.50) 15.88 (3.58) 0.13 0.900 Shrubs 3.37 (0.85) 3.20 (1.04) 0.11 0.918 7.22 (0.88) 5.76 (1.41) 0.88 0.400 27.75 (1.60) 23.88 (5.88) 0.64 0.543

Ground-layer herbs (%cover) Ferns 5.80 (2.05) 9.64 (2.68) 0.93 0.373 14.59 (3.92) 15.10 (3.63) 0.09 0.923 64.50 (17.50) 53.00 (12.32) 0.54 0.602 Fern allies 2.60 (1.25) 1.46 (0.79) 0.80 0.443 5.99 (2.55) 3.27 (1.47) 0.99 0.344 25.00 (10.21) 13.76 (6.19) 1.03 0.327 Graminoids 0.90 (0.13) 2.87 (0.56) 3.41 0.010 1.97 (0.29) 4.86 (0.78) 3.46 0.008 8.25 (1.18) 19.50 (3.23) 3.27 0.010 Spring ephemerals 0.14 (0.08) 4.38 (1.97) 1.49 0.168 0.30 (0.18) 4.48 (1.67) 1.72 0.115 1.00 (0.58) 18.13 (7.13) 1.66 0.129 Early-summer forbs 1.89 (0.53) 5.36 (2.08) 1.14 0.280 5.46 (0.58) 7.80 (2.36) 0.96 0.365 25.00 (2.04) 31.13 (8.83) 0.57 0.588 Late-summer forbs 1.55 (0.63) 5.43 (2.88) 1.32 0.226 5.02 (2.54) 9.77 (4.63) 0.90 0.390 24.00 (12.98) 33.25 (15.03) 0.39 0.702 Vines 0.33 (0.24) 0.43 (0.25) 0.25 0.806 1.29 (0.95) 1.39 (0.76) 0.08 0.942 6.25 (4.73) 6.50 (3.65) 0.04 0.968 Moss 3.80 (1.24) 2.99 (1.14) 0.44 0.670 9.91 (2.86) 7.51 (2.48) 0.59 0.569 42.50 (13.62) 30.63 (9.93) 0.70 0.502 Total herb cover 24.51 (3.79) 48.29 (9.39) 2.35 0.044 26.57 (4.49) 27.82 (3.83) 0.20 0.847 97.50 (13.75) 102.50 (14.78) 0.21 0.835

%Cover 0.58 0.578 19.41 (1.73) 14.65 (2.24) 1.38 0.197 73.75 (9.44) 53.75 (8.60) 1.43 0.183 LeafRock litter 86.22 1.51 (3.57) (0.52) 88.40 1.94 (2.02) (0.49) 0.55 0.596 4.97 (1.51) 6.09 (1.61) 0.44 0.672 22.50 (7.22) 26.50 (7.68) 0.33 0.749 CWD (>5 cm) 10.78 (1.62) 10.91 (1.38) 0.05 0.957 15.74 (1.73) 15.95 (1.74) 0.08 0.939 56.25 (6.25) 61.88 (7.56) 0.48 0.642 EMS 3.34 (1.66) 1.94 (0.86) 0.84 0.422 9.94 (3.64) 5.04 (1.88) 1.34 0.210 45.00 (16.46) 22.00 (8.24) 1.41 0.188 O-horizon depth (cm) 3.09 (0.73) 1.72 (0.26) 1.78 0.155 1.54 (0.22) 0.93 (0.17) 2.13 0.059 6.97 (1.12) 3.90 (0.72) 2.24 0.049 O-horizon weight (g) 34.27 (4.91) 29.91 (2.51) 0.89 0.396 12.18 (0.98) 11.80 (0.93) 0.25 0.804 50.37 (3.01) 50.29 (5.32) 0.14 0.888 %Light (1 m) 1.77 (0.54) 2.35 (0.90) 0.52 0.620 1.24 (0.25) 1.85 (0.83) 0.62 0.553 4.95 (0.92) 7.46 (3.56) 0.61 0.561 %Light (2 m) 2.28 (0.63) 3.78 (1.95) 0.66 0.531 1.60 (0.35) 3.94 (2.66) 0.87 0.431 5.65 (1.15) 17.76 (13.07) 0.92 0.407 Total CWD 118.63 (13.96) 91.93 (9.55) 1.60 0.141 71.85 (12.05) 63.73 (2.87) 0.89 0.393 280.52 (39.74) 247.93 (12.27) 1.02 0.333

Decay classes Class 1 (DC1) 1.31 (0.83) 1.55 (0.66) 0.22 0.832 5.11 (3.24) 3.71 (1.05) 0.53 0.610 24.07 (15.79) 15.89 (4.26) 0.50 0.647 Class 2 (DC2) 26.76 (2.88) 11.39 (2.33) 3.95 0.003 40.13 (8.44) 20.01 (3.75) 2.56 0.028 155.12 (42.61) 85.69 (15.51) 1.91 0.085 Class 3 (DC3) 25.88 (4.42) 20.97 (3.40) 0.85 0.413 28.02 (5.04) 26.66 (4.54) 0.18 0.858 102.13 (14.67) 102.42 (16.50) 0.01 0.991 Class 4 (DC4) 32.91 (5.53) 27.01 (3.84) 0.88 0.398 35.44 (6.54) 32.91 (4.20) 0.34 0.743 136.69 (21.29) 129.77 (21.39) 0.20 0.843 Class 5 (DC5) 31.77 (8.90) 31.00 (2.49) 0.08 0.938 31.58 (6.80) 34.99 (1.98) 0.63 0.541 116.04 (24.95) 132.32 (8.41) 0.62 0.572

Size classes Large (45+ cm) 31.91 (10.02) 27.29 (3.84) 0.53 0.609 42.30 (9.50) 47.05 (3.74) 0.57 0.583 142.10 (29.75) 178.51 (16.39) 1.17 0.268 Mature (25–45 cm) 51.48 (4.66) 37.65 (4.43) 1.94 0.082 40.83 (6.54) 36.60 (2.73) 0.72 0.490 173.19 (41.60) 146.23 (11.95) 0.62 0.572 Pole (10–25 cm) 32.06 (3.80) 24.31 (2.50) 1.75 0.111 20.62 (3.06) 17.30 (1.59) 1.08 0.307 78.85 (11.65) 66.37 (6.06) 1.06 0.313

Small (5–10 cm) 3.18 (0.20) 2.82 (0.45) 1.95 0.597 1.95 (0.22) 1.80 (0.23) 0.42 0.681 7.49 (1.09) 7.12 (0.86) 0.25 0.805 2556–2568 (2009) 258 Management and Ecology Forest / al. et Burton J.I.

Values are means with standard errors in parentheses. Subplot means of all characteristics were included in the first ordination of plots described by community attributes (Fig. 3).

Table 4 Comparison of dispersion of plot means, standard deviations and ranges of community attributes.

Stand-scale dispersion (subplot means) Dispersion of heterogeneity (subplot standard deviations) Dispersion of ranges (ranges of subplots)

Primary stands (n = 4) Second-growth (n =8) T Pr > jtj Primary stands (n = 4) Second-growth (n =8) T Pr > jtj Primary stands (n = 4) Second-growth (n =8) T Pr > jtj

BA 1.32 (0.42) 3.16 (0.87) 1.91 0.087 2.41 (0.24) 1.16 (0.19) 3.94 0.003 9.62 (0.29) 6.93 (0.61) 4.00 0.003 SM BA 0.76 (0.12) 5.47 (1.42) 3.32 0.013 1.70 (0.47) 1.11 (0.25) 1.22 0.251 8.89 (3.11) 4.71 (1.61) 1.34 0.211 YB TPA 10.50 (3.86) 4.44 (1.06) 1.51 0.215 11.90 (3.38) 7.06 (1.48) 1.55 0.153 4.72 (9.19) 27.85 (5.82) 1.90 0.086 Conifer BA 0.69 (0.25) 1.86 (0.30) 2.50 0.032 1.47 (0.52) 2.85 (0.50) 1.72 0.117 6.16 (3.08) 10.26 (2.73) 0.92 0.380 SM saplings 1042.47 (366.69) 4875.13 (777.81) 4.46 0.001 18777.80 (792.60) 3161.40 (733.10) 13.15 <0.001 3382.04 (669.74) 12632.93 (3225.01) 2.81 0.024 Conifer saplings 15.92 (0.01) 202.92 (61.18) 2.11 0.061 55.09 (20.00) 437.30 (106.81) 3.52 0.009 298.42 (99.47) 1691.02 (332.05) 2.87 0.017 Shrub density 1296.74 (234.29) 2314.08 (390.89) 2.23 0.050 1829.63 (498.63) 4380.66 (949.29) 1.80 0.102 7955.45 (2976.66) 18670.45 (5075.77) 1.41 0.190 Shrub cover 1.37 (0.32) 2.28 (0.59) 1.04 0.320 1.19 (0.55) 3.30 (0.66) 1.36 0.034 2.75 (0.20) 13.63 (2.85) 3.81 0.007 SE forbs 0.14 (0.03) 3.64 (1.41) 2.48 0.043 0.30 (0.03) 3.22 (1.14) 2.55 0.038 1.00 (0) 12.66 (5.29) 2.200 0.063 ES forbs 0.79 (0.27) 4.23 (1.33) 2.53 0.037 0.90 (0.26) 5.05 (1.39) 2.92 0.021 2.50 (1.44) 19.16 (5.06) 3.17 0.013 LS forbs 0.83 (0.42) 6.27 (1.64) 2.27 0.047 3.53 (1.51) 10.32 (2.50) 1.80 0.101 18.50 (7.38) 33.81 (7.90) 1.23 0.248 3.02 0.015 1.75 (0.61) 7.13 (1.79) 2.84 0.021 Graminoids 0.19 (0.07) 1.32 (0.39) 4.15 0.003 0.42 (0.15) 1.76 (0.41) O-horizon depth 1.17 (0.27) 0.55 (0.15) 2.15 0.057 0.32 (0.12) 0.35 (0.10) 0.22 0.828 1.72 (0.51) 1.55 (0.42) 0.240 0.814 %Light (2 m) 1.07 (0.13) 3.11 (1.17) 1.73 0.157 0.50 (0.19) 4.26 (1.60) 2.33 0.078 1.63 (0.66) 20.91 (7.85) 2.45 0.070 CWD DC5 14.29 (3.33) 5.57 (1.32) 2.96 0.014 11.74 (0.58) 4.10 (1.23) 5.62 <0.001 42.86 (3.13) 17.70 (5.10) 4.21 0.002 Mature CWD volume 6.51 (2.75) 10.71 (1.80) 1.31 0.219 9.75 (3.32) 6.19 (1.42) 1.18 0.267 61.83 (21.35) 22.47 (8.41) 2.09 0.063 Mature snag density 4.46 (1.84) 4.18 (1.10) 0.14 0.893 4.18 (1.58) 5.46 (1.26) 0.61 0.558 11.94 (3.98) 27.85 (5.63) 2.31 0.044

Dispersion values were calculated as the absolute difference between plot attributes and the respective group means, and provide a means to measure and compare among-stand, or landscape-scale variability (Levene, 1960), standard errors are given in parentheses. Dispersion was examined at the stand (means) and within-stand scales (standard deviations and ranges). Only those community attributes showing suggestive evidence for significant

differences in dispersion between primary and second-growth stands (p < 0.10) at any scale are shown. 2563 2564 J.I. Burton et al. / Forest Ecology and Management 258 (2009) 2556–2568

(r = 0.64), SM BA (r = 0.57), conifer seedling cover (r = 0.53), Table 5 the density of other hardwood saplings (r = 0.53), percent cover Understory plant species correlated (r 0.50) with ordination axes by guild. of leaf litter (r = 0.51) and early-summer forbs (r = 0.51) were Primary Second-growth Axis 1 Axis 2 negatively related to axis 2. Fern allies (%cover) Axis 1 contrasted second-growth stands in later stages of Lycopodium annotinum 2.53 (1.26) 0.97 (0.54) 0.55 0.43 development dominated by sugar maple with those with greater Ferns (%cover) abundances of other hardwood species; sugar maple BA (r = 0.82), Athyrium felix-femina 3.21 (0.88) 6.19 (1.76) 0.56 0.33 percent cover of sugar maple seedlings (r = 0.73), the density of sugar maple saplings (r = 0.73), %large (r = 0.63), total BA (r = 0.59), Spring ephemerals (%cover) Claytonia caroliniana 0.14 (0.08) 2.55 (0.60) 0.83 0.44 Modal D (r = 0.54) and CWD in DC3 (r = 0.52) were positively Dicentra spp. 0.00 (0.00) 0.88 (0.73) 0.59 0.53 related to axis 2 (Fig. 3) while conifer sapling density (r = 0.88), Early-summer forbs (%cover) other hardwood TPH (r = 0.83), late-summer forb cover Anenome quinquefolia 0.03 (0.03) 0.71 (0.25) 0.61 0.03 (r = 0.80), total herb cover r = 0.77), other hardwood BA Asarum canadensis 0.00 (0.00) 0.04 (0.04) 0.58 0.51 (r = 0.76), YB sapling density (r = 0.74), shrub cover Mertensia paniculata 0.00 (0.00) 0.04 (0.03) 0.68 0.48 (r = 0.74) and density (r = 0.73), conifer TPH (r = 0.72), Sanguinaria canadensis 0.00 (0.00) 0.06 (0.05) 0.51 0.21 graminoid cover (r = 0.59), conifer BA (r = 0.56), ferns and fern Streptopus roseus 1.58 (0.36) 3.02 (0.33) 0.61 0.49 Trillium spp. 0.07 (0.04) 0.27 (0.08) 0.67 0.04 allies (r = 0.53 and 0.51, respectively) were negatively related to Uvularia grandiflora 0.00 (0.00) 0.77 (0.57) 0.63 0.51 axis 1. MRPP showed that community structure varied among Viola pubescens 0.06 (0.05) 0.80 (0.29) 0.84 0.38 stands in different stages of development (p = 0.057). Pair-wise Late-summer forbs (%cover) comparisons showed that pole stands differed from mature stands Carex arctata 0.03 (0.03) 0.27 (0.10) 0.18 0.55 (p = 0.039) while mature and pole, and mature and old-growth stands did not differ (p > 0.10). In contrast, soil texture did not Shrubs 1 m tall (%cover) Lonicera canadensis 0.00 (0.00) 0.19 (0.09) 0.63 0.23 appear to be related to community structure (MRPP, p = 0.102). Ribes spp. 0.00 (0.00) 0.06 (0.04) 0.52 0.46

1 4.6. Relationships among community attributes, understory species Shrubs >1 m (stems ha ) Corylus cornuta 899.22 (570.80) 2343.5 (1059.10) <0.01 0.60 and stand origin Trees seedlings (%cover) Betula alleghaniensis 0.24 (0.08) 0.14 (0.05) 0.49 0.60 The second ordination of understory species resulted in a three- dimensional NMS solution that captured 74.4% of the total Other hardwoods variation (40.0% of the variation on axis 1, 18.9% on axis 2; Acer rubrum 0.01 (0.01) 0.14 (0.09) 0.14 0.56 Betula spp. 0.02 (0.02) 0.01 (0.01) 0.16 0.60 Fig. 3b), had a final stress of 8.60 and demonstrated greater structure than expected by chance (Monte Carlo, a = 0.05). Primary Conifers and second-growth stands exhibited strong differences in unders- Picea glauca 39.79 (15.24) 7.96 (5.21) 0.55 0.11 tory plant community composition and structure (MRPP; Cover or density estimates are given by type (mean and standard error), as well as p = 0.019). While differences between stands in different devel- Pearson correlations with plot axis scores. Taxonomic authority is Flora of North opmental stages were not substantial (MRPP; p = 0.150), stands America, 1993+. that varied in soil texture (coarse loamy vs. loamy and fine to very fine) exhibited significant differences in understory plant com- canadensis (r = 0.51), U. grandiflora (r = 0.51) and F. nigra munities (MRPP; p = 0.030). Because soil texture classes are seedlings (r = 0.51) were negatively related to axis 2. Shrub comparably distributed among primary and second-growth density (r = 0.72), CWD in DC5 (r = 0.57), elevation (r = 0.56), and stands, we do not expect these differences to impact comparison mineral soil (r = 0.52) were positively related to axis 2, and spring of these stand types. ephemerals were negatively related to axis 2 (r = 0.58). Percent Primary stands were contrasted with second-growth stands diffuse light transmittance (%light) at 2 m was positively primarily along axis 1 (Fig. 3b) and positively associated with associated with axis 2 (r = 0.76, p = 0.027), but only after the higher densities of P. glauca saplings and greater percent cover of removal of an outlying second-growth stand (BH). Lycopodium annotinum (r = 0.72 and 0.55, respectively; Table 5). Viola pubescens (r = 0.84), Claytonia caroliniana (r = 0.83), 4.7. Indicator species analysis Mertensia paniculata (r = 0.68), Trillium spp. (r = 0.67), Uvularia grandiflora (r = 0.63), Lonicera canadensis (r = 0.63), Streptopus Analysis of herbaceous (non-woody) indicator species identi- roseus (r = 0.61), Anenome quinquefolia (r = 0.61), Dicentra spp. fied four species closely associated with second-growth stands (r = 0.59), Asarum canadensis (r = 0.58), Athyrium felix-femina including one spring ephemeral (C. caroliniana; p = 0.025), and (r = 0.56), Ribes spp. (r = 0.52) and Sanguinaria canadensis three early-summer forbs (A. quinquefolia, S. roseus and V. (r = 0.51) were negatively associated with axis 1 and the pubescens; p = 0.034, 0.026, and 0.060, respectively). Only one locations of primary stands (Table 5). Characteristics indicating species, an evergreen fern ally, was marginally associated with an importance of yellow birch and conifer trees (%BA, BA and TPH) primary stands (L. annotinum)(p = 0.092). The importance value of were positively related to axis 1 and the locations of primary the indicator species was at least 40 points higher in the group that stands (r = 0.72, 0.70 and 0.67, respectively for yellow birch; and they indicate with the exception of S. roseus, which was 32 points r = 0.63, 0.72 and 0.54, respectively for conifers). Average O- higher in second-growth stands than primary stands. horizon depth (r = 0.69), O-horizon weight (r = 0.57), %BA of other hardwoods (r = 0.55) and CWD in decay class two (DC2) (r = 0.53) 5. Discussion were also positively related to axis 1. Percent cover of yellow birch (r = 0.60), and first-year birch 5.1. Overstory composition and structure (yellow birch or white birch) seedlings (r = 0.60), density of Corylus cornuta (r = 0.60), cover of A. rubrum (r = 0.56) and Carex arctata Although few structural attributes varied between primary and (r = 0.55) were positively related to axis 2, while percent cover of second-growth stands when values were aggregated across Arisaema triphyllum (r = 0.58), Dicentra spp. (r = 0.53), A. species, both yellow birch and conifer species were substantially J.I. Burton et al. / Forest Ecology and Management 258 (2009) 2556–2568 2565 more abundant within primary stands. Furthermore, at the 5.3. Understory vegetation multivariate level, primary stands were separated from second- growth stands principally by a gradient in the abundance of yellow The abundance of tree seedlings and saplings did not vary for birch and conifers such that excluding these variables (yellow sugar maple, yellow birch, conifers, other hardwoods or shrubs birch and conifer BA, %BA and TPH) from the ordination weakened between primary and second-growth stands; however, tree the differences between types (MRPP, p = 0.111). The lack of yellow seedlings and saplings were associated with the composition birch and conifers in second-growth stands may be a result of high- and the structure of the overstory (Modal D and %large) at the grade logging occurring subsequent to the cutover (Stott, 1943; multivariate level. For the first ordination of community attributes, Nyland, 1992) and the complex life histories of these species conifer and yellow birch saplings, shrub cover and shrub density (Burns and Honkala, 1990). While yellow birch and conifers were were associated with earlier stages of development along axis 1. In selectively high-graded from second-growth stands, the regenera- contrast, sugar maple seedlings and saplings were positively tion strategies for yellow birch and conifer species are also associated with Modal D, %large and stands in later developmental complex. The absence of microsites suitable for the establishment stages. While the relationship between conifer and yellow birch of light-seeded species (e.g., exposed mineral soil, tip-up mounds) saplings, and stand structure observed in the first ordination was and a lack of site preparation prior to logging could have led to low not related to light transmittance, it is feasible that the canopy may levels of regeneration following the cutover (Carlton and Bazzaz, have closed since the conifer and yellow birch saplings established. 1998; Lorenzetti et al., 2008). However, these conditions are often In contrast, yellow birch seedlings were related to axis 2, and the created during harvesting activities, particularly those that locations of primary stands and the abundance of yellow birch in occurred during the cutover. Therefore, low levels of regeneration the overstory. Shrub density, CWD in DC5, A. rubrum seedlings, following the cutover may be more strongly related to dispersal exposed mineral soil and %light was correlated with axis 2, while P. limitation following the removal of reproductively mature seed glauca was associated with axis 1, and the abundance of conifer trees. Our results conflict with previous studies that identify only trees in the second ordination (of understory species). Thus, structural and few compositional differences between old-growth disturbances that increase the availability of resources, such as and second-growth stands (Hale et al., 1999; McGee et al., 1999); light, temporarily may be necessary to maintain populations of however, our work is consistent with results from northern shade-intolerant tree species (e.g., Connell, 1979). However, the Wisconsin and upper Michigan (Goodburn and Lorimer, 1999). relationship between yellow birch seedlings and %light appears to be contingent not only on the presence of microsites (e.g., exposed 5.2. Coarse woody debris and snags mineral soil or CWD in advanced stages of decay) but also upon the presence of yellow birch seed trees in the overstory. Similarly, the The abundance and distribution of CWD and snags may vary observed association among P. glauca saplings, conifer BA and both among developmental stages and as a result of the removal of primary stands may be related to increased seed availability in tree boles during harvesting (Tyrrell and Crow, 1994). Consistent these stands. with previous studies, we observed differences in the volume and Graminoid species were more abundant in second-growth distribution of CWD among size and decay classes between stand stands, and the distribution of graminoid cover was more types. However, while we observed substantially greater varia- heterogeneous both within and among second-growth stands. bility in volume in DC5 among primary stands than second- Both white-tailed deer (Odocoileus virginianus) herbivory and growth stands, primary stands also had greater volumes on exotic earthworm invasions have been associated with an average and higher levels of within-stand spatial variability for increased importance of sedge species such as Carex pensylvanica intermediate decay and size classes. The ordination of structural in northern hardwood forests (Hale et al., 2006; Wiegmann and characteristics showed that CWD in DC3 was related to %large and Waller, 2006; Holdsworth et al., 2007a). Deer herbivory and Modal D, which indicate later stages of development. In contrast, earthworm invasion severity are both enhanced by landscape previous studies comparing old-growth forests to younger fragmentation (Augustine and Frelich, 1998; Holdsworth et al., second-growth forests reported pronounced differences in large 2007b). Because second-growth stands are closer to roads, it is size classes and substantially lower total CWD volumes for even- possible that the increase in graminoid cover, and the variability of aged second-growth stands (Goodburn and Lorimer, 1998; McGee graminoid cover within stands, is an indirect effect of road density et al., 1999). Hale et al. (1999) also observed differences between and due to the effects of earthworms and deer herbivory rather stand types in mid-size classes and suggested the relatively lower than a direct legacy of historical logging. However, increased rates of decomposition of decay-resistant coniferous trees, and variability of graminoid cover among second-growth stands larger maximum tree sizes observed in the other comparative corresponds to the greater range of developmental stages among studies led to the greater volumes of wood in larger size classes second-growth stands as well as light transmittance. Furthermore, and later stages of decay in old-growth hemlock-hardwood in the ordination of understory species, C. arctata cover and %light forests relative to stands lacking hemlock (e.g., Harmon and Hua, were positively associated with axis 2, which was also modestly 1991). negatively related to Modal D and positively related to C. The density of snags detected in our study – similar between pensylvanica cover. Thus, graminoid cover also appears to be primary and secondary stands – was higher than densities higher in stands in earlier developmental stages with higher levels reported for other old-growth stands in Minnesota (Hale et al., of light transmittance resulting in greater levels of landscape-scale 1999) but similar to values reported for old-growth forests variability for second-growth stands. elsewhere (McGee et al., 1999). High densities of snags observed The close associations among understory species, community at our sites relative to other study areas may also reflect a more attributes and guilds suggest that understory species are severe of wind-disturbance in northeastern Minnesota (D’Amato partitioning resource gradients that are driven by the composition et al., 2008); however, the discrepancy might also be related to site of the overstory and CWD volume (Fig. 3). Evergreen conifer quality as it is influenced by soil texture. Less fertile, northern sites species in the primary stands (P. glauca, T. occidentalis and A. characterized by coarser-textured soils may experience greater balsamea) may function to lower light levels and temperatures snag densities because these sites may have a higher incidence of early in the spring, reducing the abundance of spring ephemerals trunk-rotting disease (Ward et al., 1966), leading to stem breakage, and early-summer species locally. Furthermore, the high-lignin as well as a lower incidence of tree tipping (Kabrick et al., 1997). and low-nitrogen concentration of conifer foliage may function to 2566 J.I. Burton et al. / Forest Ecology and Management 258 (2009) 2556–2568 slow rates of decomposition resulting in deeper O-horizons communities. This simplification of community structure in (Melillo et al., 1982), while greater nitrogen and calcium second-growth stands may be reinforced by typical patterns of concentrations of sugar maple leaf litter functions to increase disturbance and succession, leading to stands that are less resilient rates of decomposition and nutrient cycling (Reich et al., 2005). to a changing climate, future harvesting, and other stressors. The Such relationships among overstory composition, resource avail- onset of this disparity may be associated not as much with the ability and understory community composition have been original cutover as with the subsequent high-grade logging for observed repeatedly in hemlock-hardwood forests (Mladenoff, yellow birch and conifers. However, because of our low sample size 1987; Canham et al., 1994; Beatty, 1984; Boettcher and Kalisz, and lack of time series data we do not have enough information to 1990; Ferrari, 1999). Moreover, greater volumes of CWD may correctly identify the type of model (i.e., linear, non-linear, contribute to slowing rates of decomposition and nitrogen cycling hysteresis), or locations of critical thresholds. in primary stands (Campbell and Gower, 2000). In the absence of Efforts to restore the composition, structure and processes of resource regulation by conifer species and CWD, L. annotinum may reference primary stands to second-growth northern hardwood otherwise be out-competed by spring ephemeral and early- forests should therefore focus not only on restoring a stage of summer species. Alternatively, it is possible that logging directly structural development (i.e., old growth) or level of diversity, but reduced populations of L. annotinum in second-growth forests by prioritize the establishment of a patchy distribution of yellow birch disturbing the O-horizon and surface soils, and that the association and conifer species and overstory–understory feedbacks within between ground flora and tree species composition is merely second-growth stands. This may require introducing a moderate- coincidental (Zenner and Berger, 2008). severity disturbance, and temporary successional retrogression (Woods, 2004; Hanson and Lorimer, 2007), to second-growth 5.4. Diversity and cover stand in later stages of structural development coupled with planting or direct seeding and low-intensity site preparation Second-growth stands contained 162% of the quadrat richness (Lorenzetti et al., 2008). If the system is characterized by of forest herbs of primary stands, 197% of the cover of primary hysteresis, the potential for multiple states over a range of driving stands. These results contrast nearly oppositely with those of Duffy conditions, then adequate restoration of second-growth stands and Meier (1992), who observed 165% of quadrat richness and may require restoring yellow birch and conifer abundances and 252% of the cover of second-growth stands in primary stands in the heterogeneity beyond those extant in current primary stands. southern Appalachians, as well as studies comparing post- Intermediate treatments, such as thinning, crop-tree management agricultural understory communities to mature second-growth (Perkey et al., 1994) and crown release (Singer and Lorimer, 1997) stands that were never cleared for agriculture (e.g., Vellend et al., could be used to favor these species over time, as well as to 2007). However our results are consistent with other reports from accelerate the development of old-growth stand structure after the Lake States (Metzger and Schultz, 1981, 1984; Scheller and establishment. Mladenoff, 2002), and the central Appalachians (Gilliam et al., 1995) that show increased herb diversity and cover in younger Acknowledgements stands. Greater levels of herbaceous beta diversity and a lower rate of species accumulation over area in primary stands (Fig. 2) suggest Funding for the project was provided by the National Oceanic that while logging has not decreased plant diversity in second- and Atmospheric Administration and Minnesota’s Lake Superior growth stands overall, there are differences in the processes Coastal Program. We are grateful to Lake County Forestry and The structuring diversity between primary and second-growth stands. Nature Conservancy of Minnesota, and the Manitou Collaborative Because the majority of second-growth stands are in earlier stages for making this research possible. For their contributions to the of development than primary stands, these patterns and those project we would like to thank C. Dunham, D. Spina, J.E. Peck, B. observed for tree seedlings may be partially explained by the Boyce, C. Ferguson, N. Bygd and L. Desotelle. We also thank two intermediate disturbance hypothesis (Connell, 1979). However, anonymous reviewers for helpful comments on a previous version. resource regulation by conifers and CWD, as well as heterogeneity of key attributes, and dispersal limitation may also contribute to References the differences in species accumulation rates that we observed between stand types. Arrhenius, O., 1921. Species and area. Journal of Ecology 9, 95–99. Attiwill, P.M., 1994. The disturbance of forest ecosystems – the ecological basis for 5.5. 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