Forest Ecology and Management 329 (2014) 137–147
Contents lists available at ScienceDirect
Forest Ecology and Management
journal homepage: www.elsevier.com/locate/foreco
Response of tree regeneration to experimental gap creation and deer
herbivory in north temperate forests
Jodi A. Forrester ⇑, Craig G. Lorimer, Jacob H. Dyer, Stith T. Gower, David J. Mladenoff
Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, Madison, WI 53706, USA
a r t i c l e
i n f o
Article history:
Received 27 March 2014
Received in revised form 20 June 2014
Accepted 22 June 2014
Keywords:
Acer saccharum
Canopy gaps
Height growth
Northern hardwoods
Shade tolerance
Stump sprouts
a b s t r a c t
Structural heterogeneity has become a goal of contemporary forest management, yet the effect of incorporating variable sized canopy openings characteristic of older forests on ecosystem services is still largely unknown. Single-tree selection silviculture reduces tree species diversity, and group-selection
harvests often produce inconsistent results in maintaining the proportion of species with low or intermediate shade tolerance. It is unclear how much variability is related to inherent growth rate differences
among shade tolerance classes, asymmetric competition, sprouting behavior, herbivory, and other factors. We conducted an experiment to control several of these factors. The northern hardwood study area
in north-central Wisconsin included 15 replicates of each of 3 sizes of experimental gaps (50 m2, 200 m2,
and 380 m2). Ten main plots (80 80 m2) were fenced to exclude deer. Vertical height growth of saplings
and stump sprouts was monitored for two years pre-treatment and four years post-treatment.
Overstory gaps significantly increased height growth rates, but there was no significant difference
between rates of the very shade-tolerant Acer saccharum and several midtolerant species in any gap size.
Saplings dominated the regeneration layer in small gaps. Stump sprouts were more abundant and grew
faster than saplings in large gaps, but after 4 years, A. saccharum advance regeneration still predominated
in the upper height classes. Deer had limited effects on sapling development or species composition
because tall advance regeneration was beyond their reach, but they severely affected the sprout layer.
In unfenced plots, the unpalatable Ostrya viriginiana had the tallest sprouts. Overall, midtolerant species
made up about 16% of the gap regeneration layer and appear to be increasing their proportion over time.
Height growth rates of many saplings and sprouts exceeded 50 cm per year, suggesting that successful
gap capture would be likely for both shade-tolerance groups under current environmental conditions.
The non-significant difference in growth rates between shade-tolerant and midtolerant species across
the light gradient could change as more time elapses since gap creation. However, our findings after four
years are consistent with other studies in suggesting that there may be no consistent trends in the relative growth responses of shade-tolerant and midtolerant tree species to increased light and gap size.
Ó 2014 Elsevier B.V. All rights reserved.
1. Introduction
Forest harvest regimes must be continually assessed to ensure
long-term ecosystem sustainability and a broad range of services
under increasing demands for wood products. However, the
impacts of forest management upon structural and functional
characteristics that determine ecosystem sustainability and biodiversity are not fully understood. Diversity in structure provides
greater functional diversity and contributes to a broader array of
ecosystem services (Ishii et al., 2004; Hardiman et al., 2011;
Keeton et al., 2011). Second-growth forests in the U.S. Lake States
⇑ Corresponding author. Tel.: +1 (608) 265 6321; fax: +1 (608) 262 9922.
E-mail address: [email protected] (J.A. Forrester).
http://dx.doi.org/10.1016/j.foreco.2014.06.025
0378-1127/Ó 2014 Elsevier B.V. All rights reserved.
(Minnesota. Wisconsin, Michigan) region have lower diversity of
structure, composition and microenvironments than old-growth
counterparts that were not logged at the time of Euro-American
settlement (Tyrrell and Crow, 1994; McGee et al., 1999; Crow
et al., 2002; Goodburn and Lorimer, 1998; Scheller and
Mladenoff, 2002).
Uneven-aged management has become increasingly popular on
public forest lands to partly address these concerns through implementation of ecological forestry practices and to avoid controversies associated with clearcutting (Crow et al., 1994). However,
single-tree selection can lead to a substantial loss of tree species
diversity in managed forests because relatively few species are sufficiently shade tolerant to survive and prosper in small, single-tree
gaps (Leak and Sendak, 2002; Schuler, 2004). In addition, the
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J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
presence of high white-tailed deer populations in the region can
reduce the structural and species diversity of the understory vegetation (Rooney and Waller, 2003). To better understand the effects
of structural heterogeneity on function and services, we conducted
a large, replicated field experiment to add old-growth structural
elements (gaps of various sizes and coarse woody debris (CWD))
and to control deer browsing in a second-growth northern hardwood forest (Dyer et al., 2010; Stoffel et al., 2010; Forrester et al.,
2013). In this study, we compared the tree regeneration, diversity,
and growth based on two years of pre-treatment and four-years of
post-treatment data.
The ability to foster greater understory plant diversity in these
forest ecosystems requires a quantitative understanding of minimum light requirements and opening sizes needed for species of
lower shade tolerance. But survival and growth rates across a range
of light environments are poorly known for most tree species. The
traditional understanding is that shade tolerant species have a
competitive growth advantage under low light, whereas intolerant
species have a competitive advantage under high light (e.g., Horn,
1971; Givnish, 1988). These inferences have been based to a large
extent on greenhouse studies or field studies of photosynthetic and
respiration rates of small seedlings. As saplings become larger, factors such as mutual self-shading of leaves and greater respiration
costs can alter the situation compared to small seedlings
(Givnish, 1988). More recent studies of larger saplings in forest
environments have reported a surprisingly wide range of outcomes, with the less tolerant species under a full canopy having
greater (DeLucia et al., 1998; Janse-ten Klooster et al., 2007) lesser
(Lin et al., 2002; Baltzer and Thomas, 2007), or equivalent growth
rates (Gasser et al., 2010) to those of shade-tolerant species. While
there is general agreement that the more tolerant species have
higher survival rates under shade (Valladares and Niinemets,
2008), there is no strong consensus on the validity of the conventional hypothesis that shade-tolerant species have a competitive
growth advantage under a closed canopy (Sack and Grubb, 2001;
Baltzer and Thomas, 2007; Valladares and Niinemets, 2008).
Complications also arise when relying upon shade-tolerance
theory to predict response of saplings to harvest regimes such as
single-tree and group selection. A number of studies of forest saplings across a light gradient have shown that some species with
limited shade tolerance may actually grow faster than shade-tolerant species in small as well as large gaps (Beaudet and Messier,
1998; Gasser et al., 2010). Given the documented tendency of single-tree gaps to foster dominance by shade-tolerant species, this
suggests that the effective minimum opening size for successful
gap capture by the less tolerant species is influenced by several
other aspects of forest dynamics. For example, tall advance regeneration of shade-tolerant species may induce initial competitive
inequities that may be difficult for less tolerant species to
overcome (Webb and Scanga, 2001; Povak et al., 2008; Bolton
and D’Amato, 2011). Likewise, vegetative sprouting from mature
rootstocks is often a dominant regeneration pathway in deciduous
forests, and sprouts may have a strong competitive advantage over
existing sapling advance regeneration (Dietze and Clark, 2008).
Small and medium gaps are also susceptible to lateral closure by
crown expansion of mature gap-border trees (Runkle and Yetter,
1987; Webster and Lorimer, 2005). Furthermore, shorter saplings
and sprouts are vulnerable to herbivory that may vary among species. Thus, even if shade-tolerance theory predicts a competitive
growth advantage for less tolerant species for a given sapling
height and opening size, the species may still commonly fail to
capture the gap for a host of other reasons.
These issues are sufficiently complex, and involve such a long
time frame for analysis, that a satisfactory resolution will likely
require multiple approaches with several independent lines of
evidence, including replicated experiments, retrospective studies,
chronosequences, and simulations. In this paper, we present preliminary results from a replicated, long-term experiment in which
sapling and sprout growth were monitored in gaps of three size
classes and uncut control plots in an even-aged, second-growth
northern hardwood forest. A disadvantage of the experimental
approach is that decades of observation are required before the
outcome of gap capture can be determined. But advantages of
the experimental approach include documentation of pretreatment conditions, periodic monitoring of changes over time,
documentation of trees that died at various intervals (and which
would not survive to be sampled in retrospective studies), and
experimental control over factors such as deer browsing.
Our main objective of this study was to evaluate how the survival and growth of saplings and sprouts of shade-tolerant and
midtolerant species in northern hardwood forests are affected by
gap size, as well as the presence or absence of moderately high
levels of deer browsing. Specific questions include: (1) do shadetolerant species have a competitive survival and growth-rate
advantage in small gaps, and midtolerant species in large gaps,
as predicted by traditional shade-tolerance theory? (2) does this
response change with time since disturbance? (3) how does the
growth response of vegetative sprouts compare with sapling
response? (4) how strongly do deer modify the species composition and growth rates of gap regeneration under the moderately
high deer densities typical of this region?
2. Methods
2.1. Study area
This study is a part of a larger project that was initiated to quantify the effects of canopy gap formation and coarse woody debris
on ecosystem processes in northern hardwood forests. The
280-ha study area (45° 37.40 N, 90° 47.80 W) is located in the
Flambeau River State Forest, Rusk County, north-central Wisconsin,
USA. The field site is representative of the Great Lakes forest landscape with maturing, even-aged, second-growth hardwood stands
originating after clearcutting between 1925 and 1927, based on a
sample of stem cross-sections taken about 30 cm above ground.
Most of the stems originated between 1920 and 1940, with a few
originating before 1900 that were advance regeneration released
by the clearcut. While the very shade-tolerant sugar maple (Acer
saccharum) is the principal overstory tree species (56% of stand
basal area), 42% of the basal area is comprised of species that are
either intermediate in shade tolerance (hereafter ‘midtolerant’;
Niinemets and Valladares, 2006) or tend to have sparse regeneration beneath a sugar maple canopy and appear to require canopy
gaps for successful recruitment. Midtolerant species include white
ash, (Fraxinus americiana, 12% of basal area), bitternut hickory
(Carya cordiformis, 4%), black ash (Fraxinus nigra, 4%), northern
red oak (Quercus rubra, 2%), and yellow birch (Betula alleghaniensis,
2%). Other species often dependent on sizable gaps in these forests
include basswood (Tilia americana, 16%) and red maple (Acer
rubrum, 1%). Sugar maple, white ash, bitternut hickory and
hophornbeam (Ostrya virginiana) are the most common species in
the sapling layer and sugar maple dominates the seedling layer.
The site averages 444 trees per hectare and 29 m2 ha1 basal area
for trees P10 cm diameter breast height (dbh, 1.37 m) (Burton
et al., 2011).
The site is generally mesic with level to gently sloping topography. Soils are deep silt loams (Aquic or Oxyaquic Glossudalfs) of
the Magnor, Ossmer, and Freeon series overlaying dense till (David
Hvizdak, USDA, NRCS). Soils range from moderately well drained
(Freeon) to somewhat poorly drained (Magnor and Ossmer), but
all are subject to seasonally perched or high water tables. Mean
J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
January and July air temperatures (1971–2000) are 13 and 19 °C,
respectively. The median length of the growing season is 105 days
(base temperature = 0 °C) (1971–2000). Mean annual precipitation
is 84 cm with a mean annual snowfall of 133 cm (1971–2000)
(Northeastern Rusk County, WI, USA, Midwest Regional Climate
Center http://mcc.sws.uiuc.edu). The local deer density over the
time span of this study was estimated to range from 8–15 deer
per km2 (http://dnr.wisc.gov/topic/hunt/forum/18.pdf).
2.2. Experimental design
To quantify the pre-treatment environment, three circular subplots (small, medium, and large) were established within twentyfive, 80 80 m main plots (see Fig. 1 in Dyer et al., 2010) three
years prior to the application of any experimental treatment. In
all treatments involving gap creation (n = 15 plots), a canopy gap
(area directly beneath opening as defined by Runkle, 1992) was
created in each subplot. Trees were marked for removal to create
gaps of 50 m2, 200 m2, and 380 m2 in the small, medium, and large
subplots, respectively, of the fifteen main plots. Initial gap areas
following the harvest averaged (±1 standard deviation)
46 ± 28 m2, 167 ± 50 m2, and 331 ± 61 m2 for the small, medium,
and large subplots, respectively. These span the typical observed
range of gap sizes in old-growth northern hardwoods (Runkle,
1990; Goodburn, 1996). The ratios of gap diameter to canopy tree
height averaged 0.36, 0.73, and 1.0 for the small, medium and large
subplots. An unharvested ‘‘transition zone’’ surrounds each gap,
with a width of 4, 8, and 11 m (equal to the radius of the central
zone) for the small, medium, and large subplots, respectively. An
additional ‘‘buffer zone’’ with a radius of 5 m surrounds and
separates each subplot.
Gaps were created by harvesting standing live trees in January
2007, when the soil was frozen and covered with 15–20 cm of
snow. All stems greater than 5 cm dbh in the central zones of
gap treatment plots were cut using a tracked harvester (Ponsse
Ergo, Ponsse Oyj, Vieremä, Finland) and forwarder (Ponsse Buffalo,
Ponsse Oyj, Vieremä, Finland) that were operated by a certified
master logger. All wood cut from each subplot was removed from
the gap area. In the larger study, replicated plots also have CWD
additions to approximate old-growth levels (Goodburn and
Lorimer, 1998). In August of 2007 the perimeters of five gap treatment and five control plots (entire 0.64 ha main plots) were fenced
Fig. 1. Annual extension growth of saplings in the second year post-treatment
across a diffuse light gradient estimated from hemispherical photos taken above the
apex of each sapling in the same year. Observational data are displayed for sugar
maple (diamonds), bitternut hickory (triangles) and white ash (circles). Sugar maple
growth differs significantly from bitternut hickory (p = 0.0146) and ash (p = 0.0211),
though a difference between the two midtolerant species is not detectable.
139
to exclude deer. Fences were 2.1 m tall and constructed of highdensity polypropylene with a mesh size of 45 mm 50 mm.
2.3. Data collection
2.3.1. Sapling and stump sprout measurements
We measured the diameter and heights of all saplings (full census of stems 0.5–10 cm dbh and >1.37 m in height) in the central
zones of control and gap treatment plots at the end of the growing
season in two pre-treatment years (2005 and 2006) and three posttreatment years (2007, 2008 and 2010). By conducting a full census
of the central zones, we measured saplings within the boundaries
of each full canopy gap. In treatments involving gap creation, all
saplings in the transition zones were also measured in these years.
Sample sizes were 1257 sugar maple saplings and 340 midtolerant
saplings (Table 1). Heights were measured with either an 8 m telescoping height pole or a clinometer and distance tape. In the growing season immediately following gap creation (January 2007), the
species, height and diameter of freshly cut stumps within gap
zones were recorded (n = 15 plots). The presence, number and
height of the dominant stump sprouts were measured for three
post-treatment growing seasons (2007–2009). We quantified
browse on stump sprouts by using a class system to estimate the
amount of shoot and leaf tissue missing (0–5%, 6–24%, 25–49%,
50–74%, 75–100%).
2.3.2. Assessment of seasonal solar radiation and sapling extension
growth
Hemispherical canopy photos were taken above the apex of a
random subset of saplings and sprouts in the second post-treatment year to estimate seasonal solar radiation above the terminal
leader of each individual. Photographs were taken between midJune and mid-July 2008, after leaf-out was complete, using a Nikon
Coolpix 5000 fitted with an FC-E8 fisheye lens converter camera
mounted in a self-leveling gimbal. The camera unit was hoisted
on aluminum poles above saplings with heights up to 10 m and
remotely triggered with a corded remote-control (DigiSnap 2000
[Harbortronics 2007]). Three photographs at three different exposures (bracketed with plus or minus 0.7 exposure values around
the automatically selected exposure value) were taken above each
sample individual. The camera was always oriented so the top of
each photograph faced true north. Photographs were taken under
uniform light conditions before sunrise and after sunset or on uniformly overcast days to prevent scattering of sunlight in the
images.
Extension growth for each of the four previous years was nondestructively measured for the same saplings and sprouts at the
end of the growing season in August and September by bending
over saplings and measuring distances between bud-scale scars
on the terminal shoot. The leader was defined as the branch reaching the highest point above the ground for the individual (Beaudet
and Messier, 1998). For stump sprouts, extension growth was measured as the length of the dominant sprout produced from the
point of origin on the stump to the top of the stem in the first
post-treatment growing season. Subsequent years were determined by measuring distances between bud-scale scars.
Individuals with canopy photos and extension growth measurements were randomly selected in and around canopy gaps in gap
treatment plots (n = 31 gaps from 12 plots) and in control plots
(n = 14 plots). Because many species had few saplings, only individuals of the most abundant species (sugar maple, bitternut hickory, and white ash) were selected for this analysis. Saplings with a
height >10 m or dbh >5 cm were not sampled due to constraints of
the canopy photo system and bending of the saplings for examination of the terminal leader branch. Saplings were grouped into
three height classes: class 1, <3.5 m; class 2, 3.5 to 5.49 m; class
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J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
Table 1
Sample size of sapling individuals measured for height growth prior to and four years following experimental gap creation. ANOVAs were based on mean height growth per plot,
but were weighted to reflect the distribution of individuals throughout the plots.
Species or tolerance group
Sugar maple
Midtolerants
Treatment or gap size
Central zone
Transition zone
No. plots
Mean per plot
n
No. plots
Mean per plot
n
Control
Small
Medium
Large
10
12
10
13
26
2
6
6
263
27
57
72
13
14
14
7
19
34
94.3
273
471
Control
Small
Medium
Large
8
4
4
6
8
1
5
2
68
4
18
13
8
12
12
2
6
13
16
66
155
Fig. 2. Mean annual vertical height growth of sugar maple and midtolerant saplings (includes bitternut hickory, ash species, elm species, red oak, and American basswood)
with standard errors. Year 4 is the annualized average height growth over years 3 and 4. The upper left panel is growth measured in closed canopy conditions (controls); in
subsequent panels the ‘‘controls’’ present the mean of all species. Sample sizes in Table 1.
3, >5.49 m. The height classes were chosen to maximize evenness
across the range of heights sampled. Saplings averaged 5.5 m in
height, and all species averaged at least 4.0 m in height. Sugar
maple saplings were close to the overall mean, while ash and hickory were 20–25% shorter and basswood was 43% taller.
Because of the limited number of bitternut hickory and white
ash individuals, some individuals with broken tops from the
harvest or previous injury were sampled (n = 12). There was no significant effect of damage on response relative to non-damaged
individuals, so these individuals were included in all analyses.
Stump sprout and light relationships were only studied in
fenced gap addition plots (n = 5 plots) to minimize the influence
of deer herbivory on sprout growth. Deer browse was not observed
on any of the saplings (typically taller than 2 m and beyond the
reach of deer) in unfenced plots.
In total, 361 individuals (301 saplings and 60 stump sprouts)
were sampled for shoot extension growth and measurements of
light intensity above the terminal leader. Sample sizes were
skewed towards sugar maple (n = 178) because of the limited
abundance of other species (n = 95 for bitternut hickory, 79 for
white ash, and 9 basswood sprouts).
To quantify general light conditions for each treatment, hemispherical photos were also taken in each plot at four uniform locations (1 m height) within each subplot. The locations correspond to
permanently marked quadrats in the north and south portions of
the central and transition zones (see Fig. 2 in Burton et al., 2011).
2.4. Data analysis
2.4.1. Analysis of photographs
Canopy photographs were analyzed using Gap Light Analyzer v.
2.0 (Frazer et al., 1999). For each set of three photographs, the
image with maximum contrast and the least amount of distortion
was chosen. All analyses and photograph selections were conducted by a single person to minimize and systematize any error
associated with selecting thresholds during analysis. We used the
polar projection and divided the sky regions by 36 azimuth and 9
zenith regions. Regional data regarding location, growing season
length, and elevation were further specified. Light metrics (e.g.
transmitted direct and diffuse radiation) were derived from each
photograph and used as a proxy for growing season light conditions at the apex of each sapling.
2.5. Statistical analysis
The limited abundance of midtolerant species in gaps (Table 1)
made it necessary to combine midtolerant species for some analyses, but individual midtolerant species were analyzed separately
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J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
whenever sample sizes permitted. We used linear regression to
relate extension growth and light metrics for sugar maple, bitternut hickory, and white ash saplings. Variables were logtransformed to meet the assumptions of normality and homoscedasticity of variances. Categorical variables were used in the
regression analysis of saplings and light to test for differences in
the responses among species. Due to a limited number of midtolerant stump sprouts, bitternut hickory, white ash, and American
basswood sprouts were combined for that analysis.
Multiple linear regression was used to quantify the relationship
between sapling extension growth rates (from year 2 subset) and
independent variables of gap area, light intensity, initial sapling
height (2006), pre-treatment sapling growth rate, and percent
mortality of saplings in gaps. Mortality was included from both
natural and harvest-related activity. Linear regression was also
used to analyze extension growth of sprouts as a function of stump
diameter, gap area, sapling density (in year 2: 2008) and light
intensity. Variables were log-transformed to meet the assumptions
of normality and homoscedasticity of variances. Backwards elimination was used to determine the model with the combination of
variables that best explained the variation in extension growth.
Models were also evaluated using AIC selection procedures. In all
cases the best model selected with backward elimination procedures also had the lowest AIC. All individual explanatory variables
in the ‘‘best’’ models were statistically significant at p 6 0.05.
We used nested linear mixed models to test if sapling heights
differed by treatment, zone, shade tolerance, or year. Plot was
the first level of nesting, zone was nested within plot, shade tolerance was nested within zone, and repeated measures over time
were nested within each tolerance group. Because of an incomplete
factorial structure of the design, we fit three separate models
(using PROC MIXED) to test growth differences between: (1) transition zones of gap treatments relative to controls; (2) central
zones of gap treatments relative to controls; and (3) central versus
transition zones in gap treatments. A fixed block term was
included in each model to account for subtle differences in species
composition across this site (for further explanation see Burton
et al., 2011). We used a separate linear mixed model to relate
cumulative growth to initial height and light metrics for saplings.
Logistic regression was used to model the probability of sprouting as a function of stump diameter, stump height, species, and gap
size (using PROC LOGISTIC). We used ANOVA to compare heights of
stump sprouts of different species and deer exclusion (fencing
treatments). For summer 2007, before fences were constructed,
only the main effects of block and species were tested for the influence on sprout heights. In 2008 and 2009, main and interactive
effects of block, deer exclusion (fence versus open), and species
were tested on sprout height. For comparison of growth rates
between growth forms (saplings versus stump sprouts), tests were
limited to means of species groups in fenced, gap addition plots
only (n = 5). All statistical tests were conducted using SAS v9.3
(SAS, 2010; SAS Institute Inc., Cary, NC).
Mortality rates were calculated using a negative compound
0
interest rate equation: Pn0 = 1 (1 Pn)n /n, where Pn = observed
mortality rate based on an n-year measurement period and
n0 = length of period in years for which mortality is desired (one
year in this case; Lorimer, 1981). An annual mortality rate for saplings was calculated in years 1 and 4 of the post-treatment period.
3. Results
3.1. Experimental light gradient created
Under closed canopy conditions, diffuse light above the apex of
saplings ranged from 5–10% (Table 2). Diffuse light intensity ranged from 4–38% in the experimental gaps and from 6–29% in the
surrounding transition zones. In the smallest gaps, light levels
were similar to those measured in the transition zones. Within
medium and large gaps, diffuse light levels were 2–4 times greater
than light levels in the closed canopy control conditions, with an
average of 16% in medium and 20% in the largest gaps.
3.2. Initial sapling response to light intensity
Regressions of extension growth rates vs. light intensity indicate that in the second growing season after gap creation, species
differed significantly in growth rates (F2,303 = 4.24, p = 0.015;
Fig. 1). Sugar maple responded more positively to diffuse light gradients than bitternut hickory (p = 0.015) and white ash (p = 0.021).
Bitternut hickory extension growth increased in response to
increasing light, although to a lesser degree than sugar maple.
White ash extension growth did not respond to the light gradient
and did not differ significantly from hickory (p = 0.9).
Sapling growth models with additional predictor variables
indicated that sugar maple growth was best predicted from initial
Table 2
Seasonal diffuse light levels estimated from hemispherical photos above saplings sampled within (central zone) or surrounding (transition zone) experimental variable sized
canopy gaps. Gaps were created in January 2007 and photos were taken in summer 2008. Saplings ranged in height from 1.6 to 9.5 m.
Location
N
Mean diffuse light (%)
Std error
Std dev
Minimum diffuse (%)
Maximum diffuse (%)
Control
Transition small
Transition medium
Transition large
Central small
Central medium
Central large
31
35
50
59
27
40
37
6.8
9.2
9.6
11.8
10.2
15.6
20.4
0.2
0.6
0.4
0.8
0.4
0.9
1.3
1.2
3.7
2.9
5.9
2.1
5.9
7.6
4.7
5.6
5.0
5.4
7.0
4.1
7.8
10.3
23.6
18.6
29.1
17.4
28.6
37.9
Table 3
Multiple linear regression models to predict sapling extension growth by species as a function of initial height (m), mortality (%), gap area (m2), and light intensity. Growth, light
intensity, mortality, and gap area were estimated two growing seasons after variable sized canopy gaps were created. Both predictor and response variables were log transformed
to meet normality assumption.
Species
N
Intercept
Diffuse light (%)
Initial height
Sugar maple
Bitternut hickory
White ash
147
89
67
3.719
3.493
5.539
0.691
0.605
0.114
Gap area
0.108
0.211
Mortality
Model p
Adj R2
0.571
<.0001
0.0002
0.1208
0.1446
0.1644
0.0347
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J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
Table 4
Summary of mixed effect weighted model used to analyze height growth differences
among treatments, tolerance group, and years. Due to an incomplete factorial design
we used three models to test differences among central zones of gap treatment
relative to controls (presented here), transition zones of gap treatments relative to
controls (see Appendix), and central vs. transition zones in gap treatments (see
Appendix). Bold values indicate p<0.05.
Effect
Num DF
Den DF
F value
Pr > F
Block
Treatment
Tolerance group
Trt ⁄ Tol Gr
Year
Year ⁄ Trt
Year ⁄ Tol Gr
Year ⁄ Trt ⁄ Tol Gr
2
3
1
3
2
6
2
6
16
16
16
16
106
106
106
106
0.34
4.78
0
0.08
0.59
3.05
0.64
0.9
0.7178
0.0145
0.9585
0.9711
0.5573
0.0086
0.5303
0.496
A. Sugar maple
B. Midtolerants
sapling height and diffuse light (Table 3; R2 = 0.14). Bitternut hickory growth was best predicted based on gap size and diffuse light
(R2 = 0.16). Gap area and sapling mortality best predicted ash
growth, but the relationship was weak (R2 = 0.03).
3.3. Sapling total height growth over 4 years
Vertical height growth showed a significant, though slight,
decreasing trend in the control treatment over time (Fig. 2). In general, height growth in the gaps differed significantly from the controls, though differences varied by gap size and year (Table 4; year
x treatment F = 3.05, p = 0.009). Height growth was significantly
greater in medium and large gaps relative to controls (medium
p = 0.004 and large p < 0.0001). Growth was also greater in the
medium and large gaps than the smallest gaps (medium
p = 0.066 and large p = 0.022) in the second and fourth years following treatment (p-values < 0.05). Similar patterns in height
growth differences between the transition zones and controls were
measured and are presented in the Appendix. Few significant differences in growth were measured between gap zones, with the
exception that annual growth in the first growing season was significantly greater in transition zones relative to the central zone of
the gap (p = 0.012).
In closed canopy conditions (the control treatment of this
study), 80% or more of annual growth rates were 20 cm or less,
and saplings grew an average of 20 cm in height per year (Fig. 3).
In contrast, 30–55% of sugar maple individuals and 25–66% of
midtolerant individuals grew at least 30 cm per year in gap treatments. Four years following the creation of the gaps, saplings grew
an average of 46–66 cm per year in medium sized openings and
66–70 cm per year in the largest openings. Saplings in the transitional zones surrounding the created gaps also grew at an increased
rate of 39–57 cm per year.
Shade tolerance, as a main effect or in any interaction terms,
was not a significant variable in any of the height growth models
tested (Table 4 and Appendix). To assess if differences in the initial
heights were obscuring/diluting differences in light responses
between tolerance groups, we placed individuals into two initial
height classes for a subsequent analysis. This model indicated that
cumulative sapling growth over the four-year period did differ
with light intensity (F = 5.3, p = 0.0002) and by initial height
(F = 18.6, p < 0.0001), but did not differ among shade tolerance
groups (p = 0.85). In undisturbed control plots and in transition
zones surrounding the gaps, cumulative growth rates for individuals greater than 4 m tall initially were significantly greater than
individuals less than 4 m tall (Fig. 4). However within gaps, initial
height was not influential on cumulative growth patterns (p = 0.68,
0.17, and 0.97 for small, medium and large gaps, respectively).
Fig. 3. Relative frequency of mean annual vertical height growth rates for saplings
by shade tolerance group and treatment for the last three post-treatment years
2008–2010.
Fig. 4. Cumulative 4-year sapling vertical height growth (post-treatment, all
species combined) by height class across a gap size gradient (see Table 2 for
equivalent light intensities and Fig. 2 for species list).
Fig. 5. Annual mortality of sugar maple and midtolerant saplings as a function of
diffuse light. Mortality rates are from the first and fourth year following the creation
of experimental variable-sized canopy gaps. Values are mean mortality rates and
standard errors based on 15 plots.
J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
143
3.4. Sapling mortality patterns
3.6. Comparative abundance and growth of saplings and sprouts
Gap creation had a strong but negative initial effect on sapling
survival. Average mortality rates ranged from 15–30% in gaps in
the first year following harvest (Fig. 5), compared to only 5% on
average for both shade tolerance groups in control plots. By the
fourth year post-treatment, mortality was low and similar for
control and gap conditions.
Saplings comprised 64–70% of the tree regeneration present in
the experimental gaps. Saplings made up a greater proportion than
sprouts in the small gaps (70% saplings vs. 30% sprouts) and medium gaps (64% saplings vs. 36% sprouts). In large gaps, however,
sprouts were much more prominent than saplings (62% sprouts
vs. 38% saplings).
Because saplings were present as tall advance regeneration,
differences in species composition among treatments were not
pronounced after 4 years and largely reflect pre-treatment conditions. Sugar maple was the most abundant species in all treatments, ranging from 44% of the saplings in the fenced control
plots to 63% in the fenced gap plots. Midtolerant species ranged
from 13–19% in all treatments, both beneath a closed canopy and
in the gaps. Among saplings taller than 4 m, midtolerants comprised 11% of the saplings beneath a closed canopy and 16% in
the fenced gaps.
Sapling growth was significantly affected by gap size, but not by
shade tolerance group; extension growth averaged 15 cm per year
in small gaps, 22–24 cm in medium, and 27 cm per year in large
gaps. Sprout growth was significantly greater than sapling growth;
average annual extension growth of sugar maple sprouts was
32 cm in small gaps and 40–42 cm in medium and large gaps.
Annual extension growth of midtolerant sprouts averaged 56 cm
in small and medium gaps and 66 cm in large gaps.
Height distributions of the saplings and sprouts show that
stump sprouts are important in the smallest size classes (<2 m tall)
and are surviving and growing into the next tallest size class
(2–4 m; Fig. 7). Saplings dominate the taller height strata (>2 m)
and are successfully growing into taller size classes with time.
While midtolerant individuals were not abundant in the experimental gaps, several saplings had surpassed 10 m in the 4th year
post-treatment. Midtolerant species were represented by 50
stump sprouts per hectare in the tallest class (2–4 m), and 25
saplings ha1 > 6 m.
3.5. Frequency and growth rate of stump sprouts
Half of all harvested trees (50%) produced at least one sprout.
After the 3rd year post-treatment, the probability of stumps having
surviving sprouts was a function of both stump diameter (Wald
statistic = 13.09, p = 0.0003) and species group (Wald statistic = 5.6, p = 0.061). Sprouting frequency consistently decreased
with increasing stump diameter for all species (Fig. 6). Of the
336 sugar maple stumps, 41% sprouted (42% frequency for
stumps < 50 cm diameter and 30% for stumps > 50 cm). Of the
145 stumps of midtolerant species, 64% sprouted (70% of
stumps < 50 cm and 44% of stumps > 50 cm).
Regression models of extension growth vs. light intensity indicate that midtolerant sprout growth was more strongly related to
measurements of total light availability, while sprout growth of
sugar maple was only weakly related to light intensity (Table 5).
In multiple regression models, gap area and sapling density were
significant additional variables in predicting height growth. Unexpectedly, growth of sugar maple sprouts was negatively related to
gap area, and midtolerant sprout growth was positively related to
sapling density, possibly related to the issue of visibility to deer.
3.7. Effects of deer herbivory on growth rates and species composition
Fig. 6. (A) Stump sprouting frequency in relation to stump diameter (midpoint) for
sugar maple, hophornbeam and midtolerant species in the third year after gap
creation. Numbers above each bar indicate species sample size in each diameter
class. (B) Comparison of mean stump sprout height among treatments, species and
years. Fences were erected at the end of the growing season in post-treatment year
1. Heights varied significantly by species in the initial year and by treatment x
species x year in subsequent years. Numbers of individuals are indicated above each
bar.
At the start of the experiment, many saplings of both tolerant
and midtolerant species were too tall to be browsed by deer. However, deer clearly had strong negative impacts on sprout regeneration. In the first growing season following gap creation, prior to
fencing, the mean height of sprouts ranged from 25–49 cm.
Heights varied significantly by species (F = 8.33, p < 0.0001), with
the mean height of American basswood the greatest among species
and sugar maple individuals being significantly shorter than hophornbeam and all midtolerant species.
In subsequent years, sprout heights varied by species, fencing
treatment, and year (interaction term F = 6.03, p = 0.0006), with
heights being greater in fenced treatments than unfenced. For all
species, sprout heights were significantly greater in 2009 than in
2008 in the fenced treatment (all p0 s < 0.02), but height differences
between years were not significant in the open, unfenced conditions, suggesting minimal progress in height growth in browsed
areas. By the third year post-gap creation, average sprout height
in fenced plots was 2–4 times greater than sprouts in unfenced
plots. Mean heights of sprouts in unfenced areas was <50 cm for
most species, compared to 120–220 cm in the fenced areas. Basswood sprouts were the tallest when fenced from deer, followed
by bitternut hickory, ash, hophornbeam and sugar maple. In
unfenced conditions, hophornbeam sprouts were tallest, followed
by ash, basswood, and either bitternut hickory or sugar maple,
depending on the year (Fig. 6).
The percent browse of stump sprouts was estimated for all
sprouts in the third post-treatment growing season (2009).
144
J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
Table 5
Select regression models to predict stump sprout extension growth in the second year post-treatment by tolerance group as a function of light intensity. Predictor variables were
log transformed when necessary to meet normality assumption.
Species
N
Model
F
Model p
Adj R2
Sugar maple
Midtolerants
Sugar maple
Midtolerants
32
26
32
26
361.63 + 133.43 ⁄ log(direct light)
412.657 + 520.13 ⁄ log(total light)
553.57–1.82 ⁄ gap area + 608.91 ⁄ log(total light)
1060.53 + 647.03 ⁄ log(total light) + 22.74 ⁄ log(sapling density)
2.77
4.88
4.01
4.26
0.1065
0.0369
0.0289
0.0207
0.0540
0.1691
0.1628
0.2067
Fig. 7. Height class distribution of sugar maple, midtolerant species, and hophornbeam stump sprouts and saplings (stems P1.37 m in height) in fenced gaps. Data are from
central zone of gap subplots (n = 5) only; transition zones are excluded.
The percent browse differed among species as a function of treatment (treatment species: F = 11.84, p < 0.0001). A greater percentage of sprouts had been browsed in open conditions than in
fenced plots among all species, with the exception of hophornbeam.
In unfenced treatments, 36–56% of the sprouts had died, while in
fenced treatments < 10% of the sprouts had died. For hophornbeam,
an average of 7% of the sprouts had died in both fenced and
unfenced treatments.
4. Discussion
4.1. Relative responsiveness of shade-tolerance groups to gap size
The initial 4-yr response of shade-tolerant and midtolerant species across a light intensity gradient in this study was not consistent with traditional shade-tolerance theory (e.g., Horn, 1971;
Givnish, 1988), or with the opposite findings reported in some
recent studies (e.g., Kobe et al., 1995; Walters and Reich, 1999).
Neither shade-tolerant nor midtolerant saplings had a competitive
growth rate advantage in any of the light environments by year 4,
ranging from beneath a closed canopy (maximum diffuse light 17%
of full sunlight) to large canopy gaps (330 m2 gap area and maximum 38% full sunlight). There was no clear indication of a consistent change in relative performance of the two species groups over
time. Midtolerant saplings had a nominally (but non-significantly)
higher growth rate than sugar maple in small and medium gaps by
year 4. But sugar maple was growing significantly faster than the
two most abundant midtolerant species in year 2 (Fig. 1), and
growth rates of tolerant and midtolerant species were still nearly
identical in the large gaps in the 4th year post-treatment (Fig. 2).
Midtolerant species were sparsely distributed across the plots,
and this made it difficult to analyze individual species in some
cases. However, the sample sizes across the light gradient from
closed canopy to large gaps were generally sufficient to demonstrate that midtolerant species were not growing faster than sugar
maple along any portion of the light gradient during the first
4 years after gap creation (Fig. 1, Table 4).
Also surprising is the lack of differentiation in the shapes of the
curves of height growth in response to light intensity. In traditional
shade-tolerance theory, a ‘‘crossover’’ in growth rates between tolerant and intolerant species is expected at some moderate light
intensity, with tolerant species reaching an asymptotic growth rate
at lower light intensities (Sack and Grubb, 2001; Valladares and
Niinemets, 2008). Crossovers have often been observed in field
studies of tree saplings (e.g., Kobe et al., 1995; Lin et al., 2002).
However, in our study, the curves for sugar maple and bitternut
hickory were similar in shape, and hickory displayed slower
growth rates than sugar maple across the entire light gradient.
The growth rate-light intensity relationship was also surprisingly
weak for all species; multiple regression models containing predictor variables such as diffuse light, gap area, and initial sapling
height were unable to explain more than 16% of the variation in
height growth. Only in sugar maple was initial height a significant
predictor of height growth increment. There was also no apparent
difference in mortality rates of saplings of the two species groups
across the light gradient during the post-treatment period (Fig. 5).
Valladares and Niinemets (2008) listed high relative wholeplant growth rates under shade as one of the ‘‘contested’’ traits
of shade tolerance. The great variety of growth responses among
shade-tolerance groups reported in the literature needs additional
study to identify the numerous possible reasons for the
J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
inconsistent results. Some of the apparent discrepancies may be
due to the fact that many studies are conducted on small seedlings
rather than taller saplings (Walters and Reich, 1999; Valladares
and Niinemets, 2008). In the present study and other studies on
older saplings, it is also possible that a number of years after disturbance are required before consistent differences in growth rates
begin to manifest between tolerant and midtolerant species; thus,
differences may still develop between species groups over time.
Furthermore, there also may be site-induced differences in behavior. In a study of sapling and pole trees in southern Wisconsin forests, the expected crossovers between sugar maple and
midtolerant species were observed on good sites. But on belowaverage sites, there were no crossovers, and bitternut hickory
had faster height growth than sugar maple at all height levels
above, within, and beneath a closed canopy (Hix and Lorimer,
1990). It is also possible that height growth responses may differ
from stem diameter growth or whole-plant biomass responses. In
three of the longest studies of comparative growth rates based
on diameter growth on permanent plots, responses were fairly
consistent with the traditional theory. Shade-tolerant species generally grew faster under shade and more slowly in the open than
midtolerant-intolerant species of comparable sizes over a span of
17–40 years, although there was not always a strong correlation
between long-term survival and mean growth rate under shade
(Lorimer, 1981, 1983; Lin et al., 2002).
A promising approach to resolving some of these discrepancies
was used by Goodburn (2004), who estimated light intensity at the
top of tall gap and understory saplings (4–11 m tall) in northern
hardwood forests from hemispherical photos and then felled the
saplings to measure recent height and basal-area growth. Since
the gaps (ranging from 7–1000 m2) had been created 3–15 years
previously, his results probably were not highly influenced by
any immediate physiological adjustments of saplings in response
to the gaps. His results indicated that sugar maple, hemlock, and
all of the midtolerant species had height growth vs. light intensity
curves that approached an asymptote at about 30–40% full sun, but
midtolerant species had consistently higher asymptotic growth
rates. There was little evidence of crossovers for this group of species, as midtolerant species had higher growth rates than tolerant
species at all light levels, agreeing with studies by Beaudet and
Messier (1998) and Gasser et al. (2010) but based on a larger number of midtolerant species. Basal area growth rates vs. light intensity, however, were linear and steeply increasing, and there was
little difference in basal area growth rates among shade-tolerance
groups across the light gradient. Since successful gap capture
depends heavily on maintaining fast height growth rates in tall
saplings, this approach could be valuable for understanding the
long-term effects of gap size on species composition. But given
the inconsistent results in the literature, it currently is difficult to
make any broad generalizations about relative growth rates of tolerant and midtolerant species across a light gradient. It is also possible that there is no universal trend and that relative response
varies with species and site-specific environmental factors. Results
of studies conducted in a variety of forest ecosystems indicate that
the relative importance of above- and below-ground competition
is highly related to soil conditions, and light availability is the main
controlling factor where soils are rich but belowground competition becomes dominant on low fertility soils (Ricard et al., 2003).
4.2. Relative importance of saplings and sprouts
The relative dynamics of saplings and sprouts have not been
widely investigated in deciduous forests of eastern North America.
More work has been done in Quercus-Carya forests in the central
region where most tree species are vigorous sprouters (Dietze
and Clark, 2008; Atwood et al., 2009) than in the Acer-Fagus-Betula
145
forests of the North. In this study, all the principal species we monitored had sprouted from stumps with a frequency of at least 30–
40%, even among the largest size classes. While saplings (advance
regeneration) still dominate the taller regeneration 4 years after
gap creation, stump sprouts make up more than a third of the
regeneration in medium and large gaps and may be increasing
their relative importance over time. Extension growth of sugar
maple and midtolerant sprouts in small gaps was 2–4 times greater
than for saplings, while sprouts in medium and large gaps had
extension growth 2 times greater than saplings. Whether sprouts
from small and large trees are equally viable and competitive over
a span of several decades in this ecosystem is still poorly known
and will require further study. In one of the longest available studies, Church (1960) reported that sprouting frequency of 15-cm
diameter sugar maple stumps dropped from 94% to 58% in the first
5 years after logging and dropped precipitously from 38% to 6% in
75 cm diameter stumps.
4.3. Prospects for successful gap capture by midtolerant species
While it has long been known that single-tree gaps foster heavy
dominance by shade-tolerant species (Leak and Sendak, 2002;
Schuler, 2004), a number of recent studies have demonstrated that
sizable gaps in late-successional forests provide no assurance that
midtolerant or intolerant species will make up more than a minor
proportion of the tallest saplings (e.g., Bolton and D’Amato, 2011;
Kern et al., 2013).
The relative competitive ability of tolerant and midtolerant species, however, appears to be strongly dependent on habitat characteristics. Some northern hardwood forest communities occurring
on mesic, nutrient-rich soils remain heavily dominated by sugar
maple even under many disturbance scenarios (Kotar et al.,
2002; Kern et al., 2013). But in long-term studies of New England
northern hardwoods, Leak (1999) has demonstrated that group
selection applied over a span of 60 years can result in midtolerant
and intolerant species making up about 25–33% of the forest canopy. Likewise, on mesic, but less nutrient-rich soils, the midtolerant yellow birch can comprise up to 40% of the regeneration in
group selection openings even with no special treatments such
as scarification (Webster and Lorimer, 2005). In the present study,
sugar maple is still strongly dominant in the gaps 4 years after
treatment, but the proportion of midtolerant species is moderate,
comprising 16% of the regeneration in the fenced gaps. This level
may be higher than on some other northern hardwood habitat
types probably because the seasonally perched water tables in
the study area make the sites somewhat more favorable for ash
and basswood and less favorable for sugar maple.
Successful capture of gaps by gap saplings has historically
depended on a number of factors, including gap size and shape, initial height and growth rates of gap saplings, and lateral crown
growth and height growth rates of mature gap border trees
(Runkle and Yetter, 1987; Cole and Lorimer, 2005). While the combination of all these factors makes it difficult to predict the outcome outside of a modeling approach, previous field studies and
simulation trials have suggested a high rate of successful gap capture if openings are >200 m2 and the taller gap saplings are averaging at least 50 cm in height increment per year (Cole and Lorimer,
2005; Webster and Lorimer, 2005). The current distribution of
height-growth rates suggests that growth rates of many gap saplings of both sugar maple and midtolerant species are exceeding
this level (Fig. 3), suggesting that these saplings would normally
have a good chance of successful gap capture in the 160–330 m2
gaps before these gaps can close from lateral crown expansion of
mature gap border trees. Under 20th and early 21st century climate and disturbance regimes, midtolerants might be expected
to increase over time on these sites because midtolerants sprout
146
J.A. Forrester et al. / Forest Ecology and Management 329 (2014) 137–147
more frequently than sugar maple and their sprouts have faster
growth rates (Figs. 6 and 7). However, because the ash species have
little resistance to the newly invasive emerald ash borer (Agrilus
plannipennis; Herms and McCullough, 2014), ash species will not
be a significant component of gap vegetation or the mature forest
matrix in the foreseeable future, reducing the potential contribution of midtolerants to overall species richness.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the
online
version,
at
http://dx.doi.org/10.1016/j.foreco.
2014.06.025.
References
4.4. Influence of deer browsing
Because of the presence of tall advance regeneration in the
study area, the main impact of deer to date has been on the species
composition and growth rates of the sprout layer. In unfenced
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Acknowledgements
This work was supported by the USDA CSREES National
Research Initiative (Grant No. 2006-55101-17060 and Wisconsin
DNR Division of Forestry and WI DNR Bureau of Integrated Science
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