EFFECTS OF CANOPY ADULT TREES ON SEEDLING RECRUITMENT OF

AMERICAN BEECH AND SUGAR MAPLE IN FRAGMENTED FORESTS

by

SANDRA LEIGH ALBRO

Submitted in partial fulfillment of the requirements

for the degree of Master of Science

Department of Biology

CASE WESTERN RESERVE UNIVERSITY

May, 2009 CASE WESTERN RESERVE UNIVERSITY

SCHOOL OF GRADUATE STUDIES

We hereby approve the thesis/dissertation of

______Sandra Leigh Albro

candidate for the ______degreeMaster of Science *.

(signed)______Robin Snyder (chair of the committee)

______Joseph Koonce

______David Burke

______Mark Willis

______

______

(date) ______03/30/09

*We also certify that written approval has been obtained for any proprietary material contained therein. Albro iii

Table of Contents

List of Tables...... iv

List of Figures...... v

Acknowledgments...... vi

Abstract...... vii

General Introduction...... 1

Effects of canopy adult trees on seedling recruitment of American beech and sugar maple in fragmented forests...... 5

Introduction...... 5

Methods...... 7 Site characteristics...... 7 Sampling protocol...... 9 Statistical analyses...... 11

Results...... 13 Canopy type...... 13 Forest edge distance...... 14 Environmental factors vs. forest edge distance...... 17

Discussion...... 19

Conclusion...... 22

References...... 24 Albro iv

List of Tables

Table 1: Sources of variation and P-values following ANCOVA...... 14

Table 2: Regression equations describing linear relationships between seedling response variables and plot distance from a forest edge...... 15

Table 3: Regression equations describing linear relationships between environmental factors and plot distance from a forest edge...... 17 Albro v

List of Figures

Figure 1:Simple linear regression between stem densities of American beech seedlings <1 year old versus distance from a forest edge...... 15

Figure 2: Simple linear regression between stem densities and stem height:basal diameter ratios of two age classes of sugar maple seedlings versus distance from a forest edge...... 16

Figure 3: Simple linear regression between seed densities of sugar maple and canopy openness versus distance from a forest edge...... 18 Albro vi

Acknowledgments

Enormous thanks to Paul Drewa for his mentorship throughout the bulk of this project, for his insights into justifying and designing the study, and for his guidance in finding a way to meaningfully but succinctly analyze and report the data. I thank Sheryl

Petersen for her invaluable companionship and for helpful suggestions regarding prose and ideas. Ryan Miller, Cloe Knaus, and Mike Werneiwski provided much-needed help with field work. I also thank members of my thesis committee: Joseph Koonce, David

Burke, and Robin Snyder, with special thanks to Dr. Snyder for guiding and supporting me through the completion of this project. Access to study sites was generously provided by The Holden Arboretum and Case Western Reserve University Farm—facilitated by the enthusiastic support of Mary Topa and Ana Locci, respectively—and Cuyahoga Valley

National Park. Funding was provided by Case Western Reserve University. Albro vii

Effects of Canopy Adult Trees on Seedling Recruitment of

American Beech and Sugar Maple in Fragmented Forests

Abstract

by

SANDRA LEIGH ALBRO

Canopy influence has been proposed to explain the co-dominance of American beech and sugar maple in temperate forest canopies. I hypothesized that recruitment of young beech and sugar maple stems differs beneath conspecific and heterospecific canopy adult trees and may be confounded by environmental factors or forest fragmentation. In three fragmented forest stands, I measured density and stem morphology of seedlings and beech root sprouts <2.5 cm dbh in plots positioned beneath beech and sugar maple adult trees. Mean density and stem morphology of young beech and sugar maple plants were not influenced by canopy adult tree species type. However, abiotic and biotic environmental factors, as well as distance from a forest edge, had species- and age-dependent effects on seedlings and root sprouts. I conclude that differential species responses to environmental factors at young life history stages—and not canopy influence—mediate the coexistence of beech and sugar maple. Albro 1

General Introduction

Coexistence of American beech and sugar maple

Co-dominance of American beech (Fagus grandifolia Ehrh.) and sugar maple

(Acer saccharum Marsh.) characterizes a large portion of temperate forest canopies within the Beech-Maple Forest system of eastern North America (Braun 1950). High degrees of shade tolerance relative to other canopy tree species allows young size classes of beech and sugar maple to establish and persist in dark forest understories (Canham et al. 1994, Sutherland et al. 2000). Such advance-growth seedlings and saplings may act as sources for canopy recruitment and facilitate the dominance of beech and sugar maple in relatively undisturbed forest interiors, where the persistence of less shade tolerant canopy tree species is less favored (Canham 1985, Canham 1990, Sutherland et al. 2000). Due to these similarities in shade tolerance and life histories, many studies of beech and sugar maple have focused on identifying key species differences that may account for coexistence, and not competitive exclusion, of these two species (Hane et al. 2003).

Several studies have hypothesized that beech and sugar maple coexistence emerges from the effects of adult trees (canopy influence) on patterns of canopy recruitment, resulting in more frequent canopy replacement by individuals of the same or opposite species over time (Poulson and Platt 1996). Some of these studies have found that microhabitats beneath beech and sugar maple adult trees favor the growth or survival of young heterospecific plants, which may result in reciprocal canopy replacement (Fox

1977, Cypher and Boucher 1982). However, others have found higher densities of Albro 2 conspecific saplings beneath adult trees to be more common, consistent with hypotheses of self-replacement (Forrester and Runkle 2000). Finally, it remains controversial whether canopy adult trees influence younger life history stages beneath them at all

(Poulson and Platt 1996).

Several possible mechanisms have been proposed to explain the influence of canopy adult trees on young life history stages of beech and sugar maple. Consistent with hypotheses of self-replacement are canopy effects on light availability and seed dispersal.

As a result of differing crown compositions, adult beech and sugar maple trees influence the quantity and quality of light that is transmitted into forest understories in a way that may favor the survival (Canham et al. 1994) and growth (Canham 1990) of conspecific saplings. In addition, beech and sugar maple seed densities are often higher near conspecific trees (Clark et al. 1998, McEuen and Curran 2004), although distributions of seedlings do not always show similar patterns (McEuen and Curran 2004). In contrast, canopy effects on pathogen densities, as well as direct canopy influence via allelopathy, are consistent with hypotheses of reciprocal canopy replacement. As proposed by Janzen

(1970) and Connell (1971), pathogen densities have been shown to limit seedling survival under adult trees of other frequently co-occurring temperate canopy tree species (Packer and Clay 2003, Kotanen 2007). Moreover, sugar maple seedlings have been shown to be impaired by beech, but not sugar maple, leaf leachate in a greenhouse study (Hane et al.

2003). Finally, it remains unknown whether other observed canopy influences of beech Albro 3 and sugar maple, such as soil nutrient availability (Finzi et al. 1998a, Finzi et al. 1998b,

Prescott 2002), may influence understory forest dynamics.

Effects of forest fragmentation on understory woody vegetation

Environmental gradients associated with forest edges have been repeatedly shown to affect the dynamics and structure of woody plant populations and communities

(Benítez-Malvido and Martínez-Ramos 2003, Kupfer and Runkle 2003). As fragmentation by urbanization and agriculture has increased the proportion of edge- influenced forested habitats (Wade et al. 2003), the impacts of edge-to-interior environmental gradients have become more widespread (Harper et al. 2005). Higher light levels near forest edges can alter the relative abundances of shade-tolerant woody plant species in the understory, particularly by favoring the growth of shade-intolerant and non- native plants (Whitney and Runkle 1981, Palik and Murphy 1990). In addition, alterations to edaphic factors, such as soil temperature (Saunders et al. 1998) and moisture (Gehlhausen et al. 2000), may have species-specific effects on young woody plant abundances. Finally, wind gradients lead to greater wind speeds and vorticity near forest edges (Irvine et al. 1997, Laurance 2004), which may cause mechanical stress in young woody plants that can change stem morphology within edge habitats (Mitchell

2003, Anten et al. 2005).

Fragmentation may also influence the growth and survival of young woody plants by modifying regenerative processes near forest edges. For example, canopy gap dynamics in edge habitats may differ from those within forest interiors due to changes in Albro 4 adult tree mortality—which may result in more frequent gap formation (Laurance 2004)

—as well as altered canopy replacement patterns within newly formed gaps (Kupfer et al.

1997). In addition, herbivory, seed predation, and seed dispersal near edges can be influenced by the activity of deer, birds, and small mammals, whose densities or behavior near edges may differ from that of the forest interior (Johnson and Adkisson 1985,

Alverson et al. 1988, Martin et al. 2000). Apart from animal vectors, seed dispersal patterns may also be influenced by changes to wind profiles that occur across habitat boundaries, which may change seedling distributions of some woody plant species

(Nuttle and Haefner 2005). Albro 5

Effects of Canopy Adult Trees on Seedling Recruitment of American Beech and

Sugar Maple in Fragmented Forests

Introduction

In eastern deciduous forests of North America, patterns of self- or reciprocal canopy tree replacement have been repeatedly proposed to account for the coexistence of

American beech (Fagus grandifolia Ehrh.) and sugar maple (Acer saccharum Marsh.)

(e.g., Fox 1977, Cypher and Boucher 1982, Forrester and Runkle 2000, Woods 2000).

Regeneration of these shade-tolerant tree species typically depends upon advance-growth seedlings and saplings that establish and persist under dense forest canopies (Canham

1985, Canham 1990, Sutherland et al. 2000). Seedlings and saplings may survive for several decades in the understory, during which time their growth and survival can be influenced by microhabitats under conspecific (Forrester and Runkle 2000) or heterospecific canopy adult trees (Fox 1977, Cypher and Boucher 1982). Such evidence for either self- or reciprocal canopy replacement in beech and sugar maple has been demonstrated primarily in sapling and pole size classes. However, few studies have considered canopy influences on very young life history stages of these two species, despite hypotheses that limitations on recruitment at seed and seedling stages may greatly impact forest dynamics (Hurtt and Pacala 1995, Clark et al. 1998).

The influence of beech and sugar maple canopy adult trees on understory plants may be explained by differences in numerous environmental factors, including patterns of light (Canham et al. 1994) and nutrient (Finzi et al. 1998a, Finzi et al. 1998b, Prescott Albro 6

2002) availability, seed input (Ribbens et al. 1994), and pathogen densities (Packer and

Clay 2003). Such variations in environmental factors comprise species-specific microhabitats beneath adult trees, in which the recruitment and persistence of conspecific or heterospecific seedlings may be altered (Fox 1977, Canham et al. 1994). However, species differences in canopy-induced microhabitats may also be confounded or obscured by other site factors (Prescott 2002). Nevertheless, prior studies of beech and sugar maple canopy influence have assumed species-specific differences in microhabitats beneath adult trees but have failed to quantitatively evaluate such assumptions.

Prior studies of beech and sugar maple canopy influence have also failed to consider the possible confounding effects of environmental variability associated with habitat fragmentation on understory plants. Edge-mediated environmental gradients, especially those related to light (Matlack 1994, Gehlhausen et al. 2000), can alter the structure and dynamics of shade-tolerant woody plant populations and communities

(Whitney and Runkle 1981, Palik and Murphy 1990). Moreover, changes to wind profiles that occur across habitat boundaries within fragmented landscapes may modify seed dispersal patterns (Nuttle and Haefner 2005) and adult survival (Saunders et al. 1991) of some canopy tree species within forest edge habitats. While edge-induced environmental effects have been shown to alter the distributions (Palik and Murphy 1990) and growth

(Albro et al. 2008) of seedlings, it is not clear to what extent alterations in understory vegetation result from fragmentation effects on canopy influence. Albro 7

My objective was to evaluate the influence of canopy species type on seedling densities and seedling stem growth rates in microhabitats beneath American beech and sugar maple canopy adults. At the same time, I accounted for the potentially confounding effects of canopy openness, seed input, and neighboring conspecific adult trees on seedling characteristics, as well as whether seedling characteristics were influenced by the fragmented nature of my study sites. Three questions were addressed: (1) Do seedling densities and stem morphology of beech and sugar maple differ between microhabitats under conspecific or heterospecific canopy adult trees? (2) If present, can differences in seedling densities and stem morphology beneath canopy adult trees be explained by species-specific variability in environmental factors (namely, canopy openness, seed densities, or the influence of conspecific neighboring trees)? (3) Do seedling densities and stem growth rates vary with distance from a forest edge and, if so, can such relationships be explained by edge-induced environmental gradients?

Methods

Site characteristics

My study was conducted in three temperate forest sites that are situated on the

Glaciated Allegheny Plateau of the Beech-Maple Forest region (Braun 1950). These sites are located throughout northeastern Ohio, USA, and include: (1) Cuyahoga Valley

National Park (Summit County, 41.27˚N, 81.54˚W; 214 m above sea level, 115 ha;

“CVNP”), Case Western Reserve University Farm (Cuyahoga County, 41.49˚N, 81.43˚W;

341 m, 23 ha; “Farm”), and The Holden Arboretum (Geauga County, 41.60˚N, 81.26˚W; Albro 8

351 m, 435 ha; “Holden”). Temperatures in the region average 8.9˚C annually, with mean maximum and minimum temperatures occurring in July (26.9˚C) and January (!8.8˚C), respectively (1971–2000, NCDC 2004). Mean annual precipitation is 103 cm (+ 9 cm

SE), and the amount of annual snowfall varies from 150 cm in Summit County to 238 cm in Geauga County. During the study period from 2006–2007, mean monthly temperatures were within 30-year averages; however, record snowfall in January 2007 (81 cm) contributed to total annual precipitation that was 27 cm greater than the 30-year mean.

Each of my second-growth study sites is dominated by American beech and sugar maple in the canopy. Less abundant canopy tree species include Prunus serotina,

Fraxinus americana, Acer rubrum, Quercus rubra, and Carya spp. Younger life history stages of these tree species are prevalent in the understory; less frequently encountered species include Ostrya virginiana at all sites and Hamamelis virginiana at the Farm.

Detailed land use history of my sites is not available; however, based on aerial photographs from Summit Soil and Water Conservation District, Case Western Reserve

University Farm, and Geauga County Archives, the last stand-clearing event at each site occurred prior to 1937. Mean age of beech and sugar maple canopy adults, estimated allometrically from diameter at breast height (dbh; Neely 1988), is 129 years (± 4 SE) at

CVNP, 134 years (± 5 S.E) at the Farm, and 131 years (± 5 SE) at Holden.

Each study site has an abrupt, linear forest edge " 65 m long that is bordered by a grassy field and lies adjacent to either a private residence (Farm and Holden sites) or an elevated highway (Interstate 271; CVNP). Edges were estimated to be 38 years old at Albro 9

CVNP, 33 years old at the Farm, and >70 years at Holden based on aerial photographs and Cuyahoga County tax records. Further, all 3 edges face west or southwest, approximately into the direction of prevailing winds during the period of beech and sugar maple viable seed dispersal in 2006 (August–November, NCDC 2004, Bonner and Leak

2008, Zasada and Strong 2008). Forest edge aspect was similar between sites to minimize the possible confounding effects of wind patterns that vary between windward and leeward forest edges (Li et al. 1990), which may influence distributions of wind- dispersed seeds (Greene and Johnson 1996).

Soils at the three sites consist of silt loams of the Brecksville and Hornell (Farm),

Ellsworth (CVNP and Holden), and Mahoning (Holden) series (USDA 2008). These soils are characterized by acidic silt loam topsoil with silty clay loam sublayers formed of glacial till, overlying shale, sandstone, and siltstone bedrock at depths of 50 to " 200 cm

(USDA 2008). Each site varies in slope and degree of runoff and drainage. While my site at Holden has gentle slopes (2–6%) and is poorly drained, the Farm site has gentle to steep slopes (6–70%) and is well drained. CVNP is intermediate to these two sites with moderately steep (25–50%), moderately well-drained slopes.

Sampling protocol

During July–August, 2006, I centered one 5-m diameter circular plot around the base of each of 10 American beech and 10 sugar maple canopy adult trees > 45 cm dbh that were randomly selected at each site. Trees were positioned 0–200 m from west- Albro 10 facing forest edges: 10 trees within 0–100 m and 10 trees within 100–200 m of the forest edge at each site.

From August–November, 2006, I measured seed rain within plots using 4 funnel seed traps positioned under each canopy tree (0.08 m2 total trap area/tree). Funnel seed traps have been shown in comparative studies to capture greater numbers of seeds and species than other trap designs (Kollmann and Goetze 1998, Chabrerie and Alard 2005).

My traps were constructed from modified 3-liter plastic soda bottles (16 cm diameter) and were positioned 20 cm above the ground and 1.5 m from the base of the adult tree within each plot, in each of the four intercardinal directions. Seed traps were emptied every 2–4 weeks, and all beech and sugar maple seeds were counted, identified to species, and cut open to allow for visual inspection of the embryo; a fully developed, intact embryo was considered to be viable (McEuen and Curran 2004). Because beech and sugar maple seeds generally survive in soil for no longer than a year (Hughes and

Fahey 1988), I assumed the 2006 seed crop to be the sole source of emergent seedlings during the growing season of 2007.

From June–September, 2007, I measured density and stem size of seedlings < 2.5 cm dbh in each plot. All seedlings were counted and identified to species, and stems of up to 400 randomly selected seedlings per plot were each measured for stem height and basal diameter. Seedlings were classified as < 1 year old (“new” seedlings) or > 1 year old (“older” seedlings) based on the presence of cotyledons and terminal bud scars

(Beckage et al. 2005). Albro 11

Within each plot, I also measured several environmental variables, including (1) canopy openness, (2) distance from the base of each experimental tree to the forest edge,

(3) distance from the base of each experimental tree to neighboring trees (defined as beech and sugar maple trees " 15 cm dbh, located within 10 m), and (4) dbh of neighboring trees. Canopy openness was quantified using digital hemispherical photography. During August–September, 2007, four canopy photographs were taken in each plot—one in each intercardinal direction—at a height of 1 m using a Nikon Coolpix

8700 digital camera fitted with a 7-mm Nikon FC-E9 fisheye converter lens. Photographs were taken at dusk or on uniformly cloudy days to avoid overexposure of images by direct sunlight. Canopy openness was determined for the blue color plane of each photograph using Gap Light Analyzer 2.0 software for Windows (Frazer et al. 1999).

Statistical analyses

I used ANCOVA to examine the effects of canopy type on seedling densities and stem height:basal diameter ratios in the context of a randomized block design with sampling, where sites served as blocks, and canopy openness, conspecific seed densities, and a conspecific neighboring tree influence index served as covariates. For each of two age classes of beech and sugar maple seedlings and one class of beech root sprouts, I calculated density (standardized to stems/m2) and mean stem height:basal diameter ratio in each plot. Each of these response variables were then analyzed using ANCOVA, for 10 separate analyses. Mean canopy openness was calculated from 4 hemispherical canopy Albro 12

photographs per plot. A neighboring tree influence index (If) was calculated separately for beech and sugar maple within each plot as

, where Dn is the dbh of a neighboring tree, and distn,f is the distance (# 10 m) between the experimental canopy adult tree and a neighboring tree (Woods 2000). Analysis of variance (ANOVA) was used to ensure that covariates served as continuous variables and not as class variables that were determined by canopy type.

I used simple linear regression to examine relationships between plant characteristics (stem densities and mean height:basal diameter ratios) within plots and plot distance from a forest edge. In addition, regression was used to test for relationships between continuous environmental variables (mean canopy openness, beech and sugar maple seed densities, and beech and sugar maple neighboring tree influence indices) within plots and plot distance from a forest edge. Although regression analyses lumped plots from all three study sites—thereby disregarding possible variability in response variables that could be attributed to differences among sites—the presence of significant linear relationships was confirmed using ANCOVA, where sites served as blocks. Where necessary, continuous variables were natural-log transformed to meet model assumptions.

Statistical analyses were performed using SAS version 9.1 software for Windows (SAS

2004); for all analyses, $ = 0.05. Albro 13

Results

Beneath beech and sugar maple canopy adult trees, I collected 514 beech seeds and 818 sugar maple seeds in 2006, of which 30% and 24% were viable, respectively. In addition, I encountered a total of 6,479 seedlings during the 2007 growing season. Of these, 3,389 were < 1 year old (new) and 2,387 were > 1 year old (older) sugar maple seedlings. By contrast, only 96 new and 267 older beech seedlings were encountered, along with 340 beech root sprouts.

Canopy type and environmental factors

I did not detect any effect of conspecific versus heterospecific adult canopy trees on stem densities and stem height:basal diameter ratios of either American beech seedlings and root sprouts or sugar maple seedlings (P ! 0.080; Table 1). However, young life history stages of beech and sugar maple differed in response to potentially confounding environmental factors. In particular, densities of new beech seedlings were influenced by canopy openness (P = 0.020) and beech seed density (P = 0.012), whereas older beech seedlings were only influenced by neighboring beech trees (P = 0.009; Table

1a). In contrast, American beech root sprout densities were influenced by canopy openness alone (P = 0.034). Regardless of age, densities of sugar maple seedlings were influenced by conspecific seed densities (P # 0.004) and conspecific neighboring adult trees (P # 0.028; Table 1b). Further, stem height:basal diameter ratios of sugar maple seedlings < 1 year old varied with conspecific seed densities (P = 0.041; Table 1b). Albro 14

Table 1. Sources of variation and P-values from ANCOVA that was used to examine the effects of canopy species type and covariates (canopy openness, conspecific seed density, and a conspecific neighboring tree influence index) on stem density and stem height:basal diameter for (a) two age classes of American beech seedlings and all root sprouts and (b) two age classes of sugar maple.

< 1 year old ! 1 year old Rootsprouts Source of Variation Density Height:BD Density Height:BD Density Height:BD

(a) American beech P Canopy openness 0.020 0.310 0.111 0.617 0.034 0.881 Conspecific seed density 0.012 0.144 0.176 0.866 0.646 0.470

Conspecific neighboring 0.224 0.597 0.009 1.625 0.415 0.248 tree influence index Sites Canopy type 0.282 0.703 0.243 0.696 0.080 0.665 Sites % Canopy type Plots(Sites % Canopy type)

(b) sugar maple Canopy openness 0.550 0.971 0.389 0.609 Conspecific seed density < 0.001 0.041 0.004 0.097

Conspecific neighboring 0.027 0.587 0.028 0.754 tree influence index Sites Canopy type 0.970 0.396 0.495 0.172 Sites % Canopy type Plots(Sites % Canopy type)

Forest edge distance

Densities of new American beech seedlings increased with plot distance from a west-facing forest edge (P < 0.001; Table 2a). On average, I encountered three times as many new seedlings in plots located 100–200 m into the forest interior than in plots located closer to the edge (0.13 ± 0.03 SE stems/m2 versus 0.03 ± 0.01 stems/m2, respectively; Fig. 1). In contrast, root sprout densities, densities of older seedlings (" 1 Albro 15

ln(y) = 0.001x – 0.027 Figure 1. Simple linear regression between r2 = 0.270 stem densities of American beech seedlings < 1 year old versus distance from a forest edge. Stem density data are natural log– transformed and were collected from plots positioned directly beneath canopy adult trees of American beech (open circles) and sugar maple (filled circles). P < 0.001 (Table 2a).

Table 2. Regression equations describing linear relationships between stem density or stem height:basal diameter (y) versus plot distance from a forest edge (x) for (a) American beech and (b) sugar maple. N = number of plots beneath canopy adult trees.

Dependent variable Regression equation N r2 P-value

(a) American beech < 1 year old Density (stems/m2) ln(y) = 0.001 x – 0.027 60 0.270 < 0.001 Height:basal diameter ln(y) = 0.001 x + 1.947 35 0.070 0.125

" 1 year old Density (stems/m2) ln(y) = 0.001 x + 0.069 60 0.064 0.052 Height:basal diameter ln(y) = 0.000 x + 2.111 48 0.003 0.716

Root sprouts Density (stems/m2) ln(y) = 0.000 x + 0.164 60 0.006 0.553 Height:basal diameter ln(y) = 0.000 x + 2.122 32 0.000 0.962

(b) sugar maple < 1 year old Density (stems/m2) ln(y) = 0.008 x – 0.100 60 0.204 < 0.001 Height:basal diameter ln(y) = 0.001 x + 1.810 53 0.154 0.004

" 1 year old Density (stems/m2) ln(y) = 0.005 x – 0.030 60 0.099 0.014 Height:basal diameter ln(y) = 0.002 x + 1.732 48 0.119 0.017 Albro 16

(a) ln(y) = 0.008x – 0.100 (b) ln(y) = 0.001x + 1.810 r2 = 0.204 r2 = 0.154

(c) ln(y) = 0.005x – 0.030 (d) ln(y) = 0.002x + 1.732 r2 = 0.099 r2 = 0.119

Figure 2. Simple linear regression between stem densities and stem height:basal diameter ratios of (a, b) sugar maple seedlings < 1 year old and (c, d) sugar maple seedlings " 1 year old versus distance from a forest edge. Dependent variables are natural log– transformed. American beech = open circles, sugar maple = filled circles. P-values are given in Table 2b. year old), and stem height:basal diameter relationships of all American beech classes were not affected by forest edge distance (P " 0.052; Table 2a).

Seedling densities and stem height:basal diameter ratios of both age classes of sugar maple increased with plot distance from a forest edge (P # 0.017; Table 2b).

Densities of new seedlings averaged 1 stem/m2 (± 0.3 S.E.) in plots positioned < 100 m from the edge, compared to 5 stems/m2 (± 2.0 S.E.) in plots located 100–200 m from the Albro 17 edge (Fig. 2a). In addition, new seedlings were 5.6 cm tall per mm of stem basal diameter

(+ 0.2 S.E.) in plots located < 100 m from the edge but were 11% taller per mm of stem basal diameter (± 3% S.E.) in plots situated farther into the forest (Fig. 2b). Similarly, older seedlings averaged 1 stem/m2 (± 0.4 S.E.) in plots located < 100 m from the forest edge, compared to 3 stems/m2 (± 1.0 S.E.) within plots located " 100 m from the edge (P

= 0.014, Fig. 2c). Older seedlings averaged 5.4 cm in height per mm stem basal diameter

(+ 0.4 S.E.) near the forest edge, but were 24% taller (± 9% S.E.) for a given stem basal diameter at distances " 100 m from the edge (P = 0.017; Fig. 2d).

Table 3. Regression equations describing linear relationships between canopy openness, seed density, or a neighboring tree influence index (y) versus plot distance from a forest edge (x) for (a) American beech and (b) sugar maple. N = 60 plots beneath canopy adult trees.

Dependent variable Regression equation r2 P-value

Canopy openness y = 0.008 x + 6.136 0.073 0.037

(a) American beech Seed density ln(y) = 0.000 x + 0.313 0.000 0.899 Neighboring tree influence index y = 0.000 x + 0.168 0.016 0.330

(b) sugar maple Seed density ln(y) = 0.002 x + 0.179 0.072 0.038 Neighboring tree influence index y = 0.000 x + 0.070 0.026 0.218

Environmental factors vs. forest edge distance

Both canopy openness and sugar maple seed densities increased with distance from a forest edge (P < 0.038; Table 3). Canopy openness averaged 6.5% (± 0.2 S.E.) in plots located < 100 m from the edge, compared to 7.4% (± 0.3 S.E.) in plots located Albro 18 farther into the forest (Fig. 3a). Similarly, densities of sugar maple seeds averaged 0.67 seeds/m2 (± 0.23 S.E.) in plots < 100 m from the edge, but 0.74 seeds/m2 (± 0.19 S.E.) in plots located " 100 m from the edge (Fig. 3b). Thus, compared to plots that were located closer to the edge, both canopy openness and sugar maple seed density were 10% greater in plots located 100–200 m into the forest interior.

(a) ln(y) = 0.002x + 0.179 Figure 3. Simple linear r2 = 0.072 regression between (a) canopy openness and (b) seed densities of sugar maple versus distance from a west-facing forest edge. Seed densities are natural log–transformed. Canopy openness and seed density data were collected from within the same plots. American beech = open circles, sugar maple = filled circles. P-values are given (b) y = 0.008x + 6.136 in Table 3. r2 = 0.073 Albro 19

Discussion

In my study, beech and sugar maple seedling abundances and stem characteristics did not differ beneath conspecific versus heterospecific adult trees, suggesting that canopy type does not play an important role in the recruitment or persistence of beech and sugar maple seedlings. My results do not agree with those of Cypher and Boucher

(1982), who found greater growth rates of beech and sugar maple seedlings (# 40 cm tall) under heterospecific canopy adult trees. They hypothesized that such growth differences accounted for species coexistence via reciprocal canopy replacement. However, Poulson and Platt (1996) showed that canopy-induced seedling differences in growth and size- class distributions did not persist into larger size classes of either beech or sugar maple.

Together, the results of my study and those of Poulson and Platt suggest that canopy effects on young life history stages of beech and sugar maple, if present, are not sufficient to explain coexistence of these two species.

I also found no difference in the densities and stem growth of beech root sprouts between beech and sugar maple canopy types; thus, canopy influence on vegetative reproduction in beech is not likely to facilitate beech–sugar maple coexistence. Root sprout densities can be highly spatially variable within and among sites (Held 1983, Jones and Raynal 1986), and individual root sprouts may be located up to 10 m away from the base of their parent tree (Jones and Raynal 1986). In my forest sites, where the average distance from experimental trees to nearby beech and sugar maple adult trees is 7.0 m and

7.1 m, respectively, beech root sprouts may be positioned to replace either conspecific or Albro 20 heterospecific canopy adult trees. Therefore, beech root sprout distributions do not show a directional pattern toward either self- or reciprocal replacement that would be necessary to explain coexistence via canopy influence.

Environmental factors that were associated with beech and sugar maple seedlings imply different limitations on seedling recruitment in these two species. Patterns of beech seedling emergence were influenced by light availability and seed input at my study sites.

Such patterns are consistent with seedling recruitment that is limited by both seed availability (supply limitation) and seedling establishment (establishment limitation;

Clark et al. 1998). Of these two types of recruitment limitation, supply limitation has been previously shown to be more important for recruitment of animal-dispersed tree species, including beech (McEuen and Curran 2004, Caspersen and Saprunoff 2005). In comparison, seedling recruitment in sugar maple and other wind-dispersed tree species, which have relatively higher fecundity, longer seed dispersal distance, and more even seed distributions across forest stands, has been more commonly associated with establishment limitation (McEuen and Curran 2004, Caspersen and Saprunoff 2005).

Although I did not measure substrate characteristics, which have been shown to drive establishment limitation in sugar maple (Caspersen and Saprunoff 2005), I did find that densities of both age classes of sugar maple seedlings were influenced by seed input and conspecific neighboring trees and not by canopy openness, consistent with seed limitation

(Clark et al. 1998). However, I also observed an association between seed densities and stem morphology that was unrelated to canopy openness. This may indicate density- Albro 21 dependent growth among sugar maple seedlings (Allsopp and Stock 1992) and may serve as indirect evidence for establishment limitation at my sites.

Forest fragmentation appears to have species-specific effects on beech and sugar maple seedlings at my study sites, which may have implications for the continued coexistence of these two species in forests that have been greatly fragmented throughout their range (Wade et al. 2003). I found that distance from a forest edge was positively associated with densities of new beech seedlings, as well as with densities and stem morphology of both age classes of sugar maple seedlings. The effects of fragmentation on seedling patterns may be partly explained by the observed patterns of canopy openness and sugar maple seed distributions, which also varied with distance from a forest edge at my study sites. Fragmentation effects on abiotic factors (Saunders et al. 1991, Murcia

1995), including light availability (Matlack 1993, Gehlhausen et al. 2000) and wind patterns (Li et al. 1990, Irvine et al. 1997). In turn, these changes in abiotic factors have been linked to species-specific variations in the distributions (Whitney and Runkle 1981,

Palik and Murphy 1990) and stem morphology (Albro et al. 2008) of young life history stages of woody plants along forest edge–to–interior gradients. Although wind can alter the survival of some sizes and species of adult trees near forest edges (Canham et al.

2001), I did not observe variations in sugar maple neighboring tree influence indices with distance from a forest edge. This suggests that alterations to wind patterns may have directly affected seed dispersal, and not densities of seed sources, at my study sites. Albro 22

Edge effects on seedling densities and stem morphology of both age classes of sugar maple, compared to effects on new seedling densities of beech that did not persist into the next age class, may indicate a greater sensitivity of sugar maple regeneration to forest fragmentation. However, it remains unknown whether these differences in species’ responses to fragmentation persist into older life history stages or whether such differences are present at other locations within forest remnants. These details about the effects of fragmentation on regeneration patterns of beech and sugar maple must be known before we may understand the full effects of fragmentation on canopy replacement patterns—and, ultimately, coexistence—of beech and sugar maple.

Conclusion

In lieu of theories of canopy influence as a mechanism for coexistence of beech and sugar maple, some recent studies have proposed that differential trade-offs between shade tolerance and growth plasticity within canopy gaps may explain patterns of beech– sugar maple coexistence (Canham 1989). In support of such proposals, it has been shown that the survival and growth of young beech stems are greater than those of sugar maple under closed canopies, and that beech stems may be released from growth suppression by smaller increases in light (Canham 1990, Poulson and Platt 1996). In contrast, sugar maple stems may outcompete beech in canopy gaps, resulting in coexistence of beech and sugar maple across forest stands that experience a small rate of canopy gap formation

(Canham 1985, Poulson and Platt 1996). In my study, the response of beech root sprouts and new beech seedlings to small variations in light—and the absence of such responses Albro 23 by sugar maple—are consistent with subtle species differences in shade tolerance at my sites but do not address trade-offs between shade tolerance and growth plasticity.

It has also been hypothesized that species differences in seed dispersal, coupled with spatial or temporal microsite variability, may result in species coexistence (Nathan and Muller-Landau 2000). I found consistent responses of sugar maple seedlings to variations in seed input, as well as evidence for species-specific limitations on seedling recruitment at my study sites. Such differences could result in niche differentiation at seed and seedling life history stages (Clark et al. 1998); however, it remains unknown whether such processes ultimately shape patterns of canopy replacement or facilitate coexistence of beech and sugar maple.

Finally, my results illustrate a need for better understanding of fragmentation effects on processes that underlie altered plant species abundances and distributions along forest edge-to-interior gradients (Murcia 1995, Kupfer and Runkle 2003). I observed preferential edge effects on sugar maple seedling distributions at my study sites, which may be partially explained by altered seed dispersal near forest edges. Identification of the key factors that explain such dispersal patterns, as well as the long-term effects of edge-induced changes to sugar maple regeneration, is required for the development of effective management practices for beech–maple forests in fragmented landscapes

(Murcia 1995). Albro 24

References

Albro S.L., S.M. Petersen, A.C. Bachmann, and P.B. Drewa. 2008. Effects of fragmentation on juvenile morphology of Acer saccharum Marsh. (sugar maple) in temperate forests of northeastern Ohio, USA. Forest Ecology and Management, 254: 233–238. Allsopp N., W.D. Stock. 1992. Density dependent interactions between VA mycorrhizal fungi and even-aged seedlings of two perennial Fabaceae species. Oecologia, 91: 281–287. Alverson W.S., D.M. Waller, and S.L. Solheim. 1988. Forests too deer: edge effects in northern Wisconsin. Conservation Biology, 2: 348–358. Anten N.P.R., R. Casado-Garcia, and H. Nagashima. 2005. Effects of mechanical stress and plant density on mechanical characteristics, growth, and lifetime reproduction of tobacco plants. The American Naturalist, 166: 650–660. Beckage B., M. Lavine, and J.S. Clark. 2005. Survival of tree seedlings across space and time: Estimates from long-term count data. Journal of Ecology, 93: 1177–1184. Benítez-Malvido J., M. Martínez-Ramos. 2003. Impact of forest fragmentation on understory plant species richness in Amazonia. Conservation Biology, 17: 389–400. Bonner F.T., W.B. Leak. 2008. Fagus L., beech. Pages 520–524 In F.T. Bonner, (Ed.). The Woody Plant Seed Manual (Agriculture Handbook 727) [Electronic version]. Dry Branch, GA: USDA Forest Service, National Seed Laboratory. Accessed March 21, 2009 from http://www.nsl.fs.fed.us/nsl_wpsm.html Braun E.L. 1950. Deciduous forests of eastern North America. Philadelphia, PA: The Blakiston Company. 596 pp. Canham C.D., M.J. Papaik, and E.F. Latty. 2001. Interspecific variation in susceptibility to windthrow as a function of tree size and storm severity for northern temperate tree species. Canadian Journal of Forest Research, 31: 1–10. Canham C.D. 1990. Suppression and release during canopy recruitment in Fagus grandifolia. Bulletin of the Torrey Botanical Club, 117: 1–7. Canham C.D., A.C. Finzi, S.W. Pacala, and D.H. Burbank. 1994. Causes and consequences of resource heterogeneity in forests: interspecific variation in light transmission by canopy trees. Canadian Journal of Forest Research, 24: 337–349. Canham C.D. 1989. Different responses to gaps among shade-tolerant tree species. Ecology, 70: 548–550. Canham C.D. 1985. Suppression and release during canopy recruitment in Acer saccharum . Bulletin of the Torrey Botanical Club, 112: 134–145. Albro 25

Caspersen J.P., M. Saprunoff. 2005. Seedling recruitment in a northern temperate forest: the relative importance of supply and establishment limitation. Canadian Journal of Forest Research, 35: 978–989. Chabrerie O., D. Alard. 2005. Comparison of three seed trap types in a chalk grassland: Toward a standardised protocol. Plant Ecology, 176: 101–112. Clark J.S., E. Macklin, and L. Wood. 1998. Stages and spatial scales of recruitment limitation in southern appalachian forests. Ecological Monographs, 68: 213–235. Connell J.H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Pages 298–312 In P. J. Den Boer and G. Gradwell, editors. Dynamics of populations. Oosterbeek, the Netherlands: The Advanced Study Institute on Dynamics of Numbers in Populations. Cypher J., D.H. Boucher. 1982. Beech maple coexistence and seedling growth rates at Mont St-Hilaire Quebec Canada. Canadian Journal of Botany, 60: 1279–1281. Finzi A.C., C.D. Canham, and N. Van Breemen. 1998a. Canopy tree–soil interactions within temperate forests: species effects on pH and cations. Ecological Applications, 8: 447–454. Finzi A.C., N. Van Breemen, and C.D. Canham. 1998b. Canopy tree–soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecological Applications, 8: 440–446. Forrester J.A., J.R. Runkle. 2000. Mortality and replacement patterns of an old-growth Acer-Fagus woods in the Holden Arboretum, northeastern Ohio. American Midland Naturalist, 144: 227–242. Fox J.F. 1977. Alternation and coexistence of tree species. The American Naturalist, 111: 69–89. Frazer G.W., C.D. Canham, and K.P. Lertzman. 1999. Gap Light Analyzer (GLA), Version 2.0: Imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, users manual and program documentation. Burnaby, British Columbia/Millbrook, NY: Simon Fraser University/Institute of Ecosystem Studies. Gehlhausen S.M., M.W. Schwartz, and C.K. Augspurger. 2000. Vegetation and microclimatic edge effects in two mixed-mesophytic forest fragments. Plant Ecology, 147: 21–35. Greene D.F., E.A. Johnson. 1996. Wind dispersal of seeds from a forest into a clearing. Ecology, 77: 595–609. Albro 26

Hane E.N., S.P. Hamburg, A.L. Barber, and J.A. Plaut. 2003. Phytotoxicity of American beech leaf leachate to sugar maple seedlings in a greenhouse experiment. Canadian Journal of Forest Research, 33: 814–821. Harper K.A., S.E. Macdonald, P.J. Burton, J. Chen, K.D. Brosofske, S.C. Saunders, E.S. Euskirchen, D. Roberts, M.S. Jaiteh, and P.A. Esseen. 2005. Edge influence on forest structure and composition in fragmented landscapes. Conservation Biology, 19: 768– 782. Held M. 1983. Pattern of beech regeneration in the east-central United States. Bulletin of the Torrey Botanical Club, 110: 55–62. Hughes J.W., T.J. Fahey. 1988. Seed dispersal and colonization in a disturbed northern hardwood forest. Bulletin of the Torrey Botanical Club, 115: 89–90. Hurtt G.C., S.W. Pacala. 1995. The consequences of recruitment limitation: reconciling chance, history and competitive differences between plants. Journal of theoretical biology, 176: 1–12. Irvine M.R., B.A. Gardiner, and M.K. Hill. 1997. The evolution of turbulence across a forest edge. Boundary-Layer Meteorology, 84: 467–496. Janzen D.H. 1970. Herbivores and the number of tree species in tropical forests. The American Naturalist, 104: 501–528. Johnson W.C., C.S. Adkisson. 1985. Dispersal of beech nuts by blue jays in fragmented landscapes. American Midland Naturalist, 113: 319–324. Jones R.H., D.J. Raynal. 1986. Spatial distribution and development of root sprouts in Fagus grandifolia (Fagaceae). American Journal of Botany, 73: 1723–1731. Kollmann J., D. Goetze. 1998. Notes on seed traps in terrestrial plant communities. Flora(Jena), 193: 31–40. Kotanen P.M. 2007. Effects of fungal seed pathogens under conspecific and heterospecific trees in a temperate forest. Canadian Journal of Botany, 85: 918–925. Kupfer J.A., J.R. Runkle, and G.P. Malanson. 1997. Factors influencing species composition in canopy gaps: the importance of edge proximity in Hueston Woods, Ohio. The Professional Geographer, 49: 165–178. Kupfer J.A., J.R. Runkle. 2003. Edge-mediated effects on stand dynamic processes in forest interiors: a coupled field and simulation approach. Oikos, 101: 135–146. Laurance W.F. 2004. Forest-climate interactions in fragmented tropical landscapes. Philosophical Transactions of the Royal Society of London B Biological Sciences, 359: 345–352. Albro 27

Li Z., J.D. Lin, and D.R. Miller. 1990. Air flow over and through a forest edge a steady- state numerical simulation. Boundary-Layer Meteorology, 51: 179–197. Martin F.D., Wike L.D., Paddock L.S. Role of edge effect on small mammal populations in a forest fragment. ; 2000 27 June. Report nr WSRC-TR-2000-00103. Matlack G.R. 1993. Microenvironment variation within and among forest edge sites in the eastern United States. Biological Conservation, 66: 185–194. Matlack G.R. 1994. Vegetation dynamics of the forest edge—trends in space and successional time. Journal of Ecology, 82: 113–123. McEuen A.B., L.M. Curran. 2004. Seed dispersal and recruitment limitation across spatial scales in temperate forest fragments. Ecology, 85: 507–518. Mitchell S.J. 2003. Effects of mechanical stimulus, shade, and nitrogen fertilization on morphology and bending resistance in Douglas-fir seedlings. Canadian Journal of Forest Research, 33: 1602–1609. Murcia C. 1995. Edge effects in fragmented forests: implications for conservation. Trends in Ecology & Evolution, 10: 58–62. Nathan R., H.C. Muller-Landau. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution, 15: 278–285. National Climatic Data Center [NCDC]. 2004. Climatography of the United States no. 20: Monthly station climate summaries (1971–2000), Ohio. Accessed January 13, 2009 from http://cdo.ncdc.noaa.gov/climatenormals/clim20/state-pdf/oh.pdf Neely D. 1988. Valuation of landscape trees, shrubs, and other plants. Urbana, IL: International Society of Arboriculture. 28 pp. Nuttle T., J.W. Haefner. 2005. Seed dispersal in heterogenous environments: bridging the gap between mechanistic dispersal and forest dynamics models. The American Naturalist, 165: 336–349. Packer A., K. Clay. 2003. Soil pathogens and Prunus serotina seedling and sapling growth near conspecific trees. Ecology, 84: 108–119. Palik B.J., P.G. Murphy. 1990. Disturbance versus edge effects in sugar maple-beech forest fragments. Forest Ecology and Management, 32: 187–202. Poulson T.L., W.J. Platt. 1996. Replacement patterns of beech and sugar maple in Warren Woods, Michigan. Ecology, 77: 1234–1253. Prescott C.E. 2002. The influence of the forest canopy on nutrient cycling. Tree physiology, 22: 1193–1200. Albro 28

Ribbens E., J.A. Silander Jr., and S.W. Pacala. 1994. Seedling recruitment in forests: calibrating models to predict patterns of tree seedling dispersion. Ecology, 75: 1794– 1806. SAS. 2004. SAS/STAT 9.1 User's Guide. Cary, N.C.: SAS Institute. Saunders S.C., J. Chen, T.R. Crow, and K.D. Brosofske. 1998. Hierarchical relationships between landscape structure and temperature in a managed forest landscape. Landscape Ecology, 13: 381–395. Saunders D.A., R.J. Hobbs, and C.R. Margules. 1991. Biological consequences of ecosystem fragmentation - a review. Conservation Biology, 5: 18–32. Sutherland E.K., B.J. Hale, and D.M. Hix. 2000. Defining species guilds in the Central Hardwood Forest, USA. Plant Ecology, 147: 1–20. USDA Soil Survey Staff. 2008. Web Soil Survey. Accessed January 13, 2009 from http:// websoilsurvey.nrcs.usda.gov/. Wade T.G., K.H. Riitters, J.D. Wickham, and K.B. Jones. 2003. Distribution and causes of global forest fragmentation. Conservation Ecology [online], 7(2): Article 7. Accessed March 21, 2009 from http://www.consecol.org/vol7/iss2/art7/ Whitney G.G., J.R. Runkle. 1981. Edge vs. age effects in the development of a beech maple forest. Oikos, 37: 377–381. Woods K.D. 2000. Dynamics in late-successional hemlock–hardwood forests over three decades. Ecology, 81: 110–126. Zasada J.C., T.F. Strong. 2008. Acer L., maple. Pages 204–216 In F.T. Bonner (Ed.). The Woody Plant Seed Manual (Agriculture Handbook 727) [Electronic version]. Dry Branch, GA: USDA Forest Service, National Seed Laboratory. Accessed March 21, 2009 from http://www.nsl.fs.fed.us/nsl_wpsm.html