Forest Ecology and Management 303 (2013) 148–159
Contents lists available at SciVerse ScienceDirect
Forest Ecology and Management
journal homepage: www.elsevier.com/locate/foreco
The influence of ground disturbance and gap position on understory
plant diversity in upland forests of southern New England
Marlyse C. Duguid a,⇑, Brent R. Frey b, David S. Ellum c, Matthew Kelty d, Mark S. Ashton a
a
Yale School of Forestry & Environmental Studies, New Haven, CT, United States
Department of Forestry, Mississippi State University, Mississippi State, MS, United States
c
Environmental Studies Department, Warren Wilson College, Asheville, NC, United States
d
Department of Natural Resources Conservation, University of Massachusetts, Amherst, MA, United States
b
a r t i c l e
i n f o
Article history:
Received 6 December 2012
Received in revised form 8 April 2013
Accepted 15 April 2013
Keywords:
Evenness
Forest harvesting
Herbaceous
Microsite
Richness
Soils
a b s t r a c t
The forest understory contains the majority of vascular plant diversity in eastern temperate forests, and
its diversity, composition, and dynamics contribute directly to ecosystem function. Forest managers have
traditionally viewed the understory as primarily affecting forest regeneration or wildlife habitat, but the
growing recognition of goods and services the understory provides (e.g., ecosystem function, ecological
resiliency, non-timber forest products) has increased concerns about the impacts of forest management
on understory diversity. We monitored response of understory diversity to microsite position and degree
of ground-level disturbance within experimental gaps for 10 years. We did this at four sites with distinct
soil types and topographic positions of a glacial geology in southern New England that were categorized
as (i) mesic, (ii) mid-slope, (iii) outwash, and (iv) sandy-skeletal. We analyzed differences in patterns of
species richness, Shannon diversity, and evenness across sites and through time. Understory species richness was generally enhanced by gap formation. Gap position was the primary factor influencing species
richness across all sites, but the patterns of diversity and evenness within gaps was site specific.
Ground-disturbance was influential on drier sandy sites, and more pronounced earlier in the experiment.
Temporal differences were also evident across sites, with richness stabilizing at all sites 10 years after gap
creation. The one exception was the sandy-skeletal site, which was still increasing in richness. Resource
managers interested in protecting and enhancing understory species diversity need to consider underlying site, specifically soil type when planning silvicultural treatments, as the response of the understory
community to disturbance can vary greatly with site.
Ó 2013 Published by Elsevier B.V.
1. Introduction
The importance of maintaining biodiversity has been widely
recognized at both national and international levels (U.S., 2000;
Brooks et al., 2006; UNEP, 2010). Plant diversity is a fundamental
component of ecosystem diversity, contributing to both habitat
structure and ecosystem function (Srivastava and Vellend, 2005).
In eastern deciduous forests, the majority of the vascular plant species diversity is found in the herbaceous layer (Whigham, 2004).
Diversity within the herbaceous layer increases structural complexity, which has a beneficial effect on compositional diversity
of many insects, small mammals, birds, amphibians and reptiles
(Ricketts, 1999; Dauber et al., 2003). Indeed, studies have demonstrated that the richness of birds, butterflies, and certain mammals
is better correlated with understory rather than overstory richness
⇑ Corresponding author. Address: Yale University School of Forestry and Environmental Studies, Marsh Hall, 360 Prospect St., New Haven, CT 06511, United
States. Tel.: +1 203 650 9118.
E-mail address: Marlyse.duguid@yale.edu (M.C. Duguid).
0378-1127/$ - see front matter Ó 2013 Published by Elsevier B.V.
http://dx.doi.org/10.1016/j.foreco.2013.04.018
(Ricketts, 1999). The herbaceous layer plays an important role in
ecosystem function, contributing organic matter, aiding in decomposition, and conserving nutrients (Muller and Bormann, 1976;
Peterson and Rolfe, 1982; Zak et al., 1990; Roberts and Gilliam,
1995; Muller, 2003; Falk et al., 2008).
The structure of the forest understory has direct implications for
forest succession and management. Herbaceous layer competition
influences germination, establishment, and thus, spatial arrangement of regenerating tree species (Maguire and Forman, 1983;
Berkowitz et al., 1995; George and Bazzaz, 2003). Structural characteristics, such as density of the forest understory, can determine
forest regeneration processes. For example, vigorous monodominant clonal understories, such as hayscented fern (Dennstaedtia
punctilobula Michx.) can severely inhibit regeneration (Beckage
et al., 2000; De La Cretaz and Kelty, 2002). In managed forests
biodiversity can increase economic and ecological resiliency,
productivity, and community stability (Burton et al., 1992). In many
regions, understory species provide opportunities for alternative
revenue streams through non-timber forest products (NTFPs)
(Hammett and Chamberlain, 1998). For all of these reasons forest
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management should strive to preserve and, where possible, enhance
understory plant diversity (Roberts and Gilliam, 1995).
Species diversity is driven by disturbance, forest cover type, and
site history (Bormann and Likens, 1979; Whitney and Foster, 1988;
Singleton et al., 2001; Bellemare et al., 2002; Ellum et al., 2010).
Forest harvesting can significantly alter edaphic and microclimate
conditions (through increased light, soil moisture and nutrient
availability), and in turn shape the diversity and composition of
the herbaceous layer (Bhatti et al., 2000; Gilliam, 2002; Roberts
and Gilliam, 2003; Zenner et al., 2006). Much depends on intensity
of canopy removal (amount of basal area removed or gap size) and
degree of ground disturbance. The amount of canopy removal may
alter understory diversity and composition (Reader and Bricker,
1992; Battles et al., 2001; Jackson et al., 2006), or may have limited
impacts (Hughes and Fahey, 1991; Ruben et al., 1999; Schumann
et al., 2003; Kern et al., 2006). While it is apparent that ground disturbance can substantially alter understory composition (Armesto
and Pickett, 1985; Peltzer et al., 2000; Roberts and Zhu, 2002; Frey
et al., 2003; Aikens et al., 2007), the extent of its influence on diversity in respect to increased light availability is not well understood.
There has been significant work in temperate forests examining
understory response to clearcuts with inconsistent results (see reviews by Roberts and Gilliam (2003) and Moola and Vasseur
(2008)). Many studies examining group selection treatments have
found increases in understory diversity (Jenkins and Parker, 1999;
Falk et al., 2008), although the temporal component must also be
considered. Additionally, the mechanisms driving these patterns
may shift with succession (Gilliam et al., 1995), and it is unclear
what the permanent effects of forest harvesting are on understory
diversity (Duffy and Meier, 1992; Meier et al., 1995). Many studies
only look at a moment in successional time, but examining longer
time frames is necessary to isolate treatment effects (Falk et al.,
2008). Further, understory cover and compositional change may
be more influenced by gap dynamics than diversity (Moore and
Vankat, 1986). Few studies have been able to carefully assess the
impacts of ground-disturbance intensity and gap position, using
both pre- and post-disturbance data, controlled and compared
across varying soil types over successional time.
To truly understand the biological diversity of a community
species abundance measures must be incorporated; evenness
may represent a different suite of ecological functions than species
richness (Magurran, 2004). Our objective was to examine patterns
in understory plant species diversity in response to microsite position and two levels of ground-disturbance intensity. The disturbance levels included ‘‘lethal’’ treatments (all vegetation removed
and mineral soil exposed), and ‘‘release’’ (only the overstory removed). We conducted the study at four distinct sites in southern
New England (different soils and canopy compositions) to examine
whether patterns are similar across the region’s common forest
types. We examined data over a multi-year time period to capture
successional changes in diversity. We hypothesize that both
ground layer disturbance and gap position influence understory
diversity, but expect gap position will be more influential. We predict that diversity will be highest in gap positions that offer the
greatest levels of resources (light) and the least competition (from
edge trees), and that these trends will be parallel across the four
soil types studied. Across all sites we predict diversity to increase
initially before stabilizing and then eventually decrease with resource limitations due to canopy development and shading effects.
2. Methods
2.1. Study sites
We conducted this study at four sites in southern New England
selected to represent the variety of soils found in the region. Three
are glacial till soils and one is of glacial–fluvial origin (Table 1). The
climate throughout the region is cool-temperate and humid;
approximately 110 cm of precipitation is evenly distributed
throughout the year.
The first two sites are located at Yale-Myers Forest (41°560 N,
72°70 W), a 3213-hectare research and demonstration forest in
northeastern, Connecticut. The forest belongs to the region classified as Central Hardwood–Hemlock–Pine (Westveld, 1956). The
forest consists primarily of mixed-deciduous second-growth
developing on abandoned agricultural land from the mid 19th century (Meyer and Plusnin, 1945). The topography is ridge-valley
with an elevation range between 170 m and 300 m above sea level.
The soils are glacial tills composed of moderate to well-drained
stony loams overlying bedrock. Average temperatures at YaleMyers Forest in July and January are 21.2 °C and 4.1 °C, respectively (Ashton and Larson, 1996; McKenna, 2007).
The first site, labeled ‘‘Mesic’’, has a gentle slope (<10% slope)
with an easterly aspect. Soils are well-drained coarse-loamy tills.
The canopy is composed primarily of Quercus rubra L., with components of Acer rubrum L., Acer saccharum Marsh., Betula alleghaniensis
Britton., Betula lenta L., Betula papyrifera Marsh., Carya ovata (Mill.) K.
Koch, Fraxinus americana L., Liriodendron tulipifera L., and Tsuga
canadensis L. The midstory–woody species that will never grow into
canopy trees – includes Carpinus caroliniana Walter, and Hamamelis
virginiana L. The understory is fairly diverse, with Carex spp., Aralia
nudicaulis L., and a variety of ferns (Thelypteris noveboracensis (L.)
Nieuwl., Polystichum acrostichoides (Michx.) Schott, D. punctilobula,
Athyrium filix-femina (L.) Roth) as the dominant species. The mesic
site had the highest levels of pre-treatment understory richness.
The second site, labeled ‘‘Mid-slope’’, has a slight northwest aspect (<10% slope). Soils are well-drained coarse-loamy till with
coarse unsorted rocks of varying sizes. Overstory composition is
primarily Q. rubra, the midstory consists of A.rubrum, and B. lenta
with an intermittent shrub layer of Kalmia latifolia L. The dominant
herbaceous understory species are Carex spp., D. punctilobula, and
Trientalis borealis Raf.
Table 1
Summary of the four study sites in southern New England.
Site
Location
Coordinates Elevation Soil series
(m)
Drainage class
Richnessa Canopy composition
Mesic
Yale-Myers Forest,
Eastford, CT
Yale-Myers Forest,
Eastford, CT
Cadwell Forest,
Pelham, MA
Adam’s Brook,
Amherst, MA
41°560 N,
72°070 W
41°570 W,
72°070 W
42°220 N,
72°240 W
42°230 N,
72°290 W
Well-drained to poorly
drained
Well drained to excessively
well-drained
Excessively well-drained,
heterogenous
Excessively well-drained
39 (49)
Mixed mesic hardwoods
14 (20)
14 (14)
Red oak, with mixed
hardwoods and pine
Upland oak with pine
16 (22)
White pine with oak
Mid-slope
Sandy-skeletal
Outwash
a
200
Charlton and Leicester
265
Brookfield/Brimfield and
Paxton/Montauk
Gloucester
325
90
Merrimac
Total pre-harvest understory plant species richness sampled values are followed by a first-order jackknife estimator in parentheses.
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The third site, labeled ‘‘Sandy-skeletal’’, is located in Pelham,
Massachusetts in the Cadwell Memorial Forest (42°220 N,
72°240 W). Soils are well-drained ablation till, heterogeneous with
isolated perched wetlands. Elevation is approximately 325 m, the
highest of the four sites. Overstory composition is primarily mixed
upland oak (Quercus alba L., Quercus coccinea Muench., Q. rubra,
Quercus velutina Lam.), with minor components of A. rubrum and
Pinus strobus (L.) Small. Dominant understory species include Gaultheria procumbens L., D. punctilobula, A. nudicaulis, Maianthemum
canadense Desf., Medeola virginiana L., and Uvularia sessilifolia L.
Prior to gap creation the sandy-skeletal site had the lowest understory species richness (Table 1).
The fourth site, labeled ‘‘Outwash’’, is located in the Adams
Brook Forest in Amherst, Massachusetts (42°230 N, 72°290 W) on a
kame terrace. Soils are deep, excessively well-drained, sandy outwash. With an elevation of approximately 90 m, the outwash site
is the lowest of the four sites. The overstory consists primarily of
P. strobus. Common understory plants include Chimaphila maculata,
Lycopodium spp., M. canadense, and Carex spp. Average temperatures at the Massachusetts sites in July and January are 22.1 °C
and 4.6 °C, respectively (McKenna, 2007).
2.2. Experimental design
At each site, during the summer of 1999 we delineated a rectangular area 108 m 30 m running east–west to serve as the experimental gap. The experimental gaps were harvested the following
winter (1999–2000), removing all vegetation greater than 2 m in
height. We designed the gap with the intention to create a light
gradient including understory conditions, side shade, and direct
sun. We left a 15 m buffer at both the eastern and western ends
of the gap with no plots to mitigate east–west edge effects. Within
the gap there were four parallel east–west environmental zones–
north edge, north center, south center, and south edge. In addition,
there were two zones located 5 m from the northern and southern
gap edges in the adjoining forest understory parallel to the center
and edge zones. Each of the six zones had four blocks of three contiguous rectangular plots 4 m 6.5 m. Our study included two
treatment plots (lethal and release) randomly assigned within each
block, totaling 48 plots per site. The third plot was part of another
study examining planted tree seedling response and not included
in this study (McKenna, 2007). Measurement plots 2 m 4 m were
centrally located within each treatment plot to limit edge effects.
We laid out plots in 1999 and took initial measurements prior to
canopy removal and site treatments.
All sites were harvested using a Timbco feller-buncher (Timbco
Hydraulics, Shawano, WI). To minimize ground disturbance
machinery traveled between the strips. As much material was carried off site as possible; remaining slash was arranged between the
two center zones of the gap avoiding measurement plots. We treated the vegetation in the lethal plots with glyphosate herbicide
(RoundupÒ, Monsanto Corporation, St. Louis, MO) in June 2000,
and four weeks later followed up by scarifying the soil surface.
Scarification was achieved by mixing the organic pad with mineral
soil to 10 cm in depth with root rakes. The release plots received no
additional ground-level treatment. We installed a 60 high electric
fence for deer exclusion around the perimeter of the study site,
and inspected and repaired every spring for the first 6 years of
the study. Qualitative observations revealed no noticeable difference in browse between fenced and unfenced areas, and in the
summer of 2006 the fencing was removed.
2006 and 2010. Additionally, we visited the sites in early spring
to assure no spring ephemeral species were missed during summer
sampling. We identified herbaceous and shrubby plants to species
level for the majority of specimens. We used congeners for grasses,
sedges, and mosses – and in rare cases used morpho-species. When
we did use morpho-species we were confident that they were different than all other species sampled. We used USDA–NRCS for
nomenclature (USDA, 2013), and recorded percent cover using
the six point scale described by Daubenmire (1959).
2.4. Data analysis
The four sites in this study are not true replicates, therefore we
individually analyzed each site as a case study. To examine diversity response we performed two-way analysis of variance (ANOVA)
models for species richness (total count of species per plot), ShanP
non diversity (H0 = Ri¼1 pi log pi ), and evenness (J0 = H0 /ln S). Our
variables were ground-disturbance, gap position, and disturbance gap position. Individual models were run for each site, in
each post-harvest year (2002, 2004, 2006, and 2010). We carried
out Tukey HSD post hoc comparisons on gap position to determine
which positions were different from others. We assumed normality
when / > .01 in Shapiro–Wilk normality tests. We ran non-parametric Kruskal–Wallis tests on both richness and Shannon
diversity for each variable on pre-harvest (1999) data to look for
pre-existing trends. We estimated total site richness and compared
trends across sites using first-order jackknife richness estimators.
We also examined species abundance curves based on bootstrapping with 100 permutations (Magurran, 2004). To visualize
changes in richness and evenness we constructed rank abundance
curves for each site by year. All statistics were carried out using R
2.11.1 (R Development Core Team, 2010) with the additional packages Vegan and BiodiversityR (Kindt and Coe, 2005; Oksanen et al.,
2010).
3. Results
3.1. Richness: across sites and time
In the mesic site we identified 39 species prior to gap creation,
which increased after harvesting to 79 in 2002, 74 in 2004, and 86
in 2006. The highest richness observed was at 89 species in 2010, a
128% increase over pre-harvest levels. Throughout the study a total
2.3. Field sampling
We sampled each plot in the summer of 1999 before the harvest, and then subsequently once each summer in 2002, 2004,
Fig. 1. Trends in total site understory plant species richness over time as estimated
with a first-order jackknife estimate. 1999 Indicates pre-treatment levels, gap
creation in 2000.
M.C. Duguid et al. / Forest Ecology and Management 303 (2013) 148–159
151
Fig. 2. Species accumulation curves showing extrapolated number of total understory plant richness based on bootstrapping with 100 permutations (±2SD) for each site.
Initial levels (1999) are shown in gray, 10 years after gap creation (2010) is shown in black.
of 129 species (including unidentified specimens) were observed.
Percent cover of the majority of species was low, with the exception of Carex pennsylvanica Lam., ferns (e.g. Dennstaedtia punctilobula; T. noveboracensis), and Rubus spp. The only species present
in 1999 that failed to appear again were Impatiens capensis Meerb.,
and Smilax rotundifolia L., of these only S. rotundifolia was present
at more than two plots initially.
At the mid-slope site there were 14 species present before gap
creation, which increased after harvesting to 36 in 2002, peaking in
2004 with 38 species (171% increase), then declining to 37 species
in 2006, and 33 in 2010. Overall, 62 different species were identified at this site throughout the study. Amphicarpaea bracteata (L.)
Fernald, C. maculata (L.) Pursh, G. procumbens, and P. acrostichoides
were present only during the pre-harvest sampling, and only in
one or two plots.
At the sandy-skeletal site we identified 14 species prior to gap
creation, which increased to 25 in 2002, 28 in 2004, and 26 in
2006. Greatest richness was observed in 2010 with 44 species, a
214% increase over pre-harvest richness. Forty-eight species were
observed over the study and no species that were initially present
disappeared completely after the disturbance.
Finally, at the outwash site, 16 species were present initially,
increasing to 37 in 2002, and to 42 in both 2004 and 2006. Again,
greatest richness was observed in 2010 with 44 species, a 175% increase over pre-harvest levels. In total 62 species were observed
during the course of the study. The only species present pre-harvest to disappear from the site was Spiraea alba Du Roi.
Total site richness via jackknife estimation exhibited differences
in successional trends in richness amongst sites. At the mesic and
mid-slope sites species richness peaks in 2006 and begins to level
then decrease. At the two drier sites (sandy-skeletal and outwash)
richness continued to increase (Fig. 1). Species accumulation
curves show differences in slope and magnitude between preand post-treatment richness across sites, with trends are similar
to the jackknife estimates. The two drier sites have flatter slopes
in 1999, but become steeper than the moister till sites by 2010
(Fig. 2).
3.2. Richness: gap position and disturbance
With one exception (sandy-skeletal, 2002), gap position was a
significant predictor of species richness for all sites in all post-harvests years (Table 2). In the mesic, sandy-skeletal and outwash
sites the general trend in all post-harvest years was greatest richness in the southern edge and southern center gap positions, and
lowest in the understory positions (Fig. 3 & Table 3). The only significant pre-disturbance trend was in the sandy-skeletal site,
where richness increased toward the northern gap positions,
which is opposite of the post-harvest pattern at that site. The
mid-slope site showed opposite results of all other sites, with
greatest diversity values in the center and northern locations.
Intensity of ground disturbance was only significant on the sandy-skeletal site initially after harvest (2002), but on the outwash
site lethal ground disturbance produced higher species richness
in 2004, 2006, and 2010 (Table 2). On the two drier, sandy sites
lethal treatments had higher species richness initially; no difference by disturbance treatment was observed for the mesic and
mid-story sites. Only the outwash site showed consistently higher
richness on the lethal treatments throughout the study. The only
interaction effect was on the mid-slope site in 2006.
3.3. Shannon diversity
The effect on Shannon diversity was less consistent across sites
than species richness. On the mesic site disturbance type was
important initially, and then the influence of gap position became
more important – first as an interaction in 2004, then gap position
only for 2006 and 2010. The mid-slope site was opposite with gap
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M.C. Duguid et al. / Forest Ecology and Management 303 (2013) 148–159
Table 2
Significant ANOVA results for species richness, Shannon diversity, and evenness.
Year
Factora
DfN
DfD
Sum sq.
Mean sq.
F
Pr(>F)
Mesic
Species richness
2002
2004
2006
2010
GAP
GAP
GAP
GAP
5
5
5
5
15
15
15
15
384.00
350
589.00
477.35
76.90
69.90
117.70
95.47
8.65
4.04
8.03
6.61
0.00
0.02
0.00
0.00
Shannon diversity
2002
2004
2006
2010
DIST
GAP DIST
GAP
GAP
1
5
5
5
18
18
15
15
1.31
2.45
2.37
3.25
1.305
0.49
0.48
0.65
5.6
4.23
4.18
10.34
0.03
0.01
0.01
0.00
J evenness
2002
2004
2006
2010
DIST
GAP DIST
GAP DIST
GAP
1
5
5
5
18
18
18
15
0.186
0.2889
0.1326
0.10
0.1864
0.06
0.02651
0.02
11.7
6.59
3.96
4.43
0.00
0.00
0.01
0.01
2010
GAP
GAP
GAP
GAP DIST
GAP
5
5
5
5
5
15
15
15
18
15
118.7
86.9
56.9
38.9
95.6
23.74
17.38
11.37
7.77
19.1
4.3
5.05
6.54
2.82
3.98
0.01
0.01
0.00
0.05
0.02
Shannon diversity
2002
2004
2006
2010
GAP
DIST
–
–
5
1
–
–
15
18
–
3.43
0.568
–
–
0.69
0.57
–
–
4.12
4.68
–
–
0.02
0.04
–
–
2004
2006
2010
GAP
DIST
GAP
–
–
5
1
5
–
–
15
18
15
–
–
0.98
0.25
0.6
–
–
0.2
0.25
0.12
–
–
6.75
6.9
3.58
–
–
0.00
0.02
0.03
–
–
Sandy-skeletal
Species richness
2002
2004
2006
2010
DIST
GAP
GAP
GAP
1
5
5
5
18
15
15
15
133.3
89.6
74.1
94.8
133.3
17.92
14.82
18.95
31.79
5.04
3.59
6.15
0.00
0.01
0.03
0.00
Shannon diversity
2002
2004
2006
2010
–
–
–
GAP
–
–
–
5
–
–
–
15
–
–
–
0.75
–
–
–
0.15
–
–
–
3.67
–
–
–
0.02
GAP
DIST
GAP
DIST
GAP DIST
GAP
GAP DIST
GAP DIST
5
1
5
1
5
5
5
5
15
18
15
18
18
15
18
18
0.28
0.18
0.23
0.02
0.06
0.17
0.13
0.05
0.06
0.18
0.05
0.02
0.01
0.03
0.03
0.01
4.86
16.96
8.74
6.38
3.28
8.08
5.39
5.14
0.01
0.00
0.00
0.02
0.03
0.00
0.00
0.00
GAP
GAP
DIST
GAP
DIST
GAP
DIST
5
5
1
5
1
5
1
15
15
18
15
18
15
18
169.4
227.4
20
202
27
190
50
33.9
45.5
20.02
40.4
27
38
50
9.57
14.7
6.28
7.39
4.42
3.07
8.9
0.00
0.00
0.02
0.00
0.05
0.04
0.01
GAP
DIST
GAP
GAP
5
1
5
5
15
18
15
15
3.41
1.4
3.86
2.41
0.68
1.4
0.77
0.48
3.66
6.26
14.2
3.49
0.02
0.02
0.00
0.03
Mid-slope
Species richness
2002
2004
2006
J evenness
2002
J evenness
2002
2004
2006
2010
Outwash
Species richness
2002
2004
2006
2010
Shannon diversity
2002
2004
2006
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M.C. Duguid et al. / Forest Ecology and Management 303 (2013) 148–159
Table 2 (continued)
Year
Factora
DfN
2010
–
–
GAP
DIST
GAP
GAP
–
5
1
5
5
–
J evenness
2002
2004
2006
2010
a
DfD
15
18
15
15
–
Sum sq.
Mean sq.
F
Pr(>F)
–
–
–
–
1.85
0.59
0.47
0.84
–
0.37
0.59
0.09
0.17
–
18.1
10.27
5.63
11.4
–
0.00
0.00
0.00
0.00
–
Significant factors in the model, GAP indicates microsite position; DIST indicates intensity of ground disturbance.
position significant in 2002 followed by disturbance type in 2004
(Table 2). The sandy-skeletal site showed gap position significant
only in 2010 with no disturbance effects. The outwash site was
similar to the mesic site, with disturbance type significant only
immediately post-harvest (2002), and gap position significant in
2002, 2004, and 2006 (Table 2). Across all sites the general trends
were similar for Shannon diversity as for species richness, but the
differences were less pronounced or absent.
3.4. Species evenness
On the mesic site evenness followed the same pattern as Shannon diversity, with disturbance initially important, followed by its
interaction with gap position, and then eventually only gap position (Figs. 4 and 5). Additionally, gap position was significant in
nearly all post-harvest years among the other sites. Decreasing
by 2006 at the mid-slope site, and then across the other sites by
2010. Evenness was highest in the shadiest gap positions (northern
understory and southern understory) and lowest in the sunniest
positions (north central and northern edge) across all sites. Disturbance was significant immediately post-harvest (2002) across all
sites, only on the sandy-skeletal site was it significant beyond
2004. Interaction effects were evident on the sandy-skeletal site
in 2004, 2006, and 2010 (Table 2).
Rank abundance plots show different evenness responses to
disturbance type across sites (Fig. 6). The mesic, mid-slope, and
sandy-skeletal sites all initially had a few species with higher
abundance than the majority of species present, while the outwash
site exhibited a higher level of initial evenness. The lines diverge
post-harvest for all sites, but the magnitude and effect is different
across sites.
On the mesic site the two species with the highest ranking –
Carex spp. and New York fern (T. noveboracensis) had maintained
or regained their dominance by 2010. Interestingly, Carex spp.
had lower abundance in the final sampling, while the majority of
species experienced higher abundance than pre-harvest. The
mid-slope site had less difference between pre and post-harvest
curves. Similar to the mesic site, the dominant species, hay-scented
fern (D. punctilobula), maintained its dominance, although mountain laurel (K. latifolia) increased in dominance to ranked secondsupplanting starflower (T. borealis) and Carex spp. The pre- and
post-harvest curves converge around the 20th ranked species with
low abundances seen across the majority of species. The sandyskeletal site had fewer species initially; therefore, the post-harvest
curve is longer and they never converge. A few species share
slightly higher abundances than on the mid-slope and outwash
sites, wintergreen (G. procumbens) holds a prominent place on both
curves (first in 1999, second in 2010). Interestingly, hay-scented
Fig. 3. Mean understory species richness by gap position for all sites in 2006. Gap positions are SU – southern understory, SE – southern edge, SC – southern center, NC –
northern center, NE – northern edge, and NU – northern understory. Error bars represent one standard error. Within each site, columns sharing the same letter are not
significantly different (Tukey HSD). 2006 demonstrates the pattern seen across all post-harvest years.
154
M.C. Duguid et al. / Forest Ecology and Management 303 (2013) 148–159
Table 3
Mean (standard error) plot level species richness for each year by gap position and disturbance type. For each year, columns sharing the same letter are not significantly different
(Tukey HSD).
a
1999a
2002
2004
Mesic
SU
SE
SC
NC
NE
NU
Lethal
Release
Total
6.63 (0.68)
7.5 (0.76)
6.38 (0.91)
6 (0.73)
7.63 (0.53)
6.63 (1.02)
6.33 (0.48)
7.25 (0.4)
6.79 (0.32)
12.5 (0.87)
19.5 (1.1)
18.13 (1.89)
15.63 (0.75)
13 (0.6)
12.25 (0.7)
15.33 (0.88)
15.04 (0.79)
15.19 (0.59)
13.75
21.63
19.25
18.88
15.25
15.88
18.08
16.79
17.44
Mid-slope
SU
SE
SC
NC
NE
NU
Lethal
Release
Total
2.88 (0.67)
2 (0.57)
2 (0.73)
3 (0.68)
3.38 (0.26)
4.13 (0.23)
2.63 (0.39)
3.17 (0.28)
2.9 (0.24)
4.25
6.13
9.25
7.38
8.13
7.25
7.04
7.08
7.06
Sandy-skeletal
SU
SE
SC
NC
NE
NU
Lethal
Release
Total
5.25 (0.7)
6 (0.19)
6.88 (0.55)
6.63 (0.46)
7.38 (0.46)
7.13 (0.61)
6.71 (0.35)
6.38 (0.29)
6.54 (0.23)
Outwash
SU
SE
SC
NC
NE
NU
Lethal
Release
Total
2.88 (0.67)
3.13 (0.23)
2.5 (0.33)
1.75 (0.31)
3 (0.5)
3.25 (0.41)
2.83 (0.25)
2.67 (0.27)
2.75 (0.18)
2006
2010
13.88 (1.41)
24.13 (1.66)
22.88 (1.57)
19 (1.09)
17.75 (1.52)
16.88 (1.34)
19.75 (1.1)
18.42 (1.05)
19.08 (0.76)
13.25 (1.83)
20.25 (2.02)
22.5 (0.98)
17.38 (1.87)
15.63 (1.35)
15.13 (0.72)
18.38 (1.18)
16.38 (0.91)
17.38 (0.75)
5.5 (0.71)
7.75 (0.88)
9.13 (0.67)
9.38 (0.68)
8 (0.46)
9.25 (0.62)
8.58 (0.48)
7.75 (0.44)
8.17 (0.33)
6.5 (0.63)
8.13 (0.55)
9 (0.94)
8.25 (0.62)
9.88 (0.77)
9.38 (0.56)
8.88 (0.52)
8.17 (0.34)
8.52 (0.31)
5.38 (1.9)
7 (2.47)
5.75 (2.03)
5.75 (2.03)
8.5 (3.01)
9 (3.18)
6.67 (0.48)
7.13 (0.49)
6.9 (0.34)
7.38 (0.91)
10.38 (0.84)
10.25 (0.9)
7.75 (0.84)
8.38 (1.27)
8.13 (1.08)
7.04 (0.47)
10.38 (0.5)
8.71 (0.42)
8.88 (0.79)
12.38 (0.68)
12.38 (0.89)
12 (0.78)
10.88 (0.72)
9.63 (0.68)
10.67 (0.54)
11.38 (0.45)
11.02 (0.35)
9.5 (0.33)
13.25 (0.62)
10.88 (0.9)
12.75 (0.45)
12 (0.46)
11.25 (1.01)
11.38 (0.45)
11.83 (0.45)
11.6 (0.32)
8.5 (0.19)
13.13 (0.61)
10.38 (0.32)
11.5 (0.76)
11.38 (1.02)
11.38 (1.03)
12.33 (0.55)
11.38 (0.41)
11.85 (0.35)
3.5 (0.5)
6.13 (1.08)
8.63 (1)
6.25 (0.67)
3.25 (0.67)
4.25 (0.88)
5.63 (0.68)
5.04 (0.5)
5.33 (0.42)
5.25 (0.73)
11.25 (0.75)
9.5 (0.93)
8.25 (0.98)
5.75 (0.92)
6.13 (1.04)
8.33 (0.63)
7.04 (0.69)
7.69 (0.47)
5.88 (0.72)
11.13 (0.67)
9.25 (1.11)
9.5 (1.07)
6.38 (0.94)
5.88 (1.04)
8.75 (0.72)
7.25 (0.58)
8 (0.47)
4.88 (0.91)
10.38 (0.65)
8.13 (1.22)
8.75 (1.54)
5.5 (0.78)
5.75 (1.35)
8.25 (0.67)
6.21 (0.76)
7.23 (0.52)
(0.53)
(0.79)
(0.96)
(1)
(0.97)
(0.31)
(0.57)
(0.53)
(0.39)
(1.44)
(1.98)
(1.08)
(0.74)
(1.01)
(0.83)
(0.82)
(0.94)
(0.62)
Pre-harvest observations.
fern, which holds second place pre-harvest, does not rank in the
top three in 2010. The largest discrepancy in curves is on the outwash site. The initial curve indicates an even community with the
most abundant species, spotted wintergreen (C. maculata) and Canada mayflower (M. canadense), holding only a small dominance
over the other species when compared to the other sites. Post-harvest trends show Carex spp. and moss with higher abundance than
any pre-harvest species. Subsequent species abundances decrease
slowly until it converges with the pre-harvest line around the
20th ranked species, similar to the mid-slope site (Fig. 6).
4. Discussion
Our results suggest that underlying site conditions, specifically
soil type, and potentially aspect, affect the way understory plant
diversity will respond to ground disturbance and light availability.
Gap formation alters the physical understory environment, creating resource gradients; the asymmetry of light in temperate forest
gaps interacts with soil moisture and nutrient availability to define
the floristic pattern of these gradients (McKenna, 2007). We found
gap position (light availability) as the strongest driver of post-disturbance species diversity regardless of soil type, although the
underlying patterns within these gaps are site specific. We did
not find other studies to corroborate our findings, suggesting that
more research is needed isolating different disturbance parameters
in forest harvesting.
We expected that maximum diversity would be in the position
that minimized competition and maximized resources (Connell,
1978). The south-center strip has high light availability and high
available moisture and nutrients due to no competition from the
surrounding canopy. Although not all research corroborates this,
North et al. (2005) found understory richness to be negatively
correlated with direct light. At 41–42°N latitudes the northern
edge is the brightest, driest, and therefore harshest environment
(Oliver and Larson, 1996; Gray et al., 2002; McKenna, 2007), thus
we expected lower diversity in that position. Interestingly, the
two moister till sites had opposite patterns of diversity, and
neither peaked in center positions. The mesic site had highest
diversity along the southern edge, and the mid-slope along the
north edge and understory. Depending on gap size and latitude
light may penetrate into the understory adjacent to gaps, but
even in the brightest gap positions the duration of direct sun is
brief (Canham et al., 1990). The discrepancy of the mid-slope’s
diversity pattern may be explained by: (1) The pre-harvest species composition may have provided species with a competitive
advantage in that microsite position; (2) The northern aspect
may have provided protection from spring desiccation along the
M.C. Duguid et al. / Forest Ecology and Management 303 (2013) 148–159
155
Fig. 4. Mean evenness by gap position for all sites in 2004. Gap positions are SU – southern understory, SE – southern edge, SC – southern center, NC – northern center, NE –
northern edge, and NU – northern understory. Error bars represent one standard error. Within each site, columns sharing the same letter are not significantly different (Tukey
HSD).
Fig. 5. Interaction plots of mean evenness over time by gap position and ground-disturbance (4A Mesic, 4B Sandy-skeletal). Gap positions are SU – southern understory, SE –
southern edge, SC – southern center, NC – northern center, NE – northern edge, and NU – northern understory. Ground disturbance levels are RE – release and LE – lethal.
Asterisks indicate that significant interaction in the ANOVA.
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M.C. Duguid et al. / Forest Ecology and Management 303 (2013) 148–159
Fig. 6. Rank abundance curves for all sites. Pre-harvest (1999) shown in black diamonds, 10 years post-harvest (2010) shown in gray triangles.
normally harsh northern gap edge; or (3) The resource heterogeneity in the stony till soil provides greater resource availability
than uniform soils (McKenna, 2007). The fact that the two sandy
soils followed a similar pattern to the mesic site confirms that
competition from regenerating trees is an influential spatial driver of understory plant diversity. Evenness on the other hand
peaked in the shadiest understory positions and was lowest along
the harsh, competitive north central and northern edge positions.
Dominance in those positions by a few strong competitors is
likely responsible for the low observed diversity, and is an important consideration for forest management.
Many studies have examined herbaceous layer response to gaps
with mixed results. Some found little to no relationship between
opening size and herbaceous response, and species richness unaffected by gap dynamics (Moore and Vankat, 1986; Collins and Pickett, 1988; Reader and Bricker, 1992). Others found differences in
species composition (Matlack, 1994; Schumann et al., 2003; Fahey
and Puettmann, 2007; Naaf and Wulf, 2007), supporting the theory
of resource partitioning within gaps. These differences could be explained by gap size; larger gaps possess larger resource gradients
and as a result, show more differentiation by species (Fahey and
Puettmann, 2007). Understory species composition may represent
a better reflection of these resource gradients than associated overstory species, because of their greater diversity and niche partitioning (Matlack, 1994; Fahey and Puettmann, 2007). Our results,
standardized by gap size and orientation across sites, suggest that
the underlying site conditions are important.
Disturbance may interact with microenvironment on these sites
to create a secondary axis of diversification and provide additional
opportunities for certain species to establish and contribute to further gap partitioning (Fahey and Puettmann, 2007). While size,
shape, and orientation of gaps determine resource availability (Collins et al., 1985), our results show that location and underlying site
conditions also have an effect on species diversity and sensitivity
to different levels of disturbance. Interestingly, we found that the
intensity of ground disturbance, when combined with increased
light, plays a more important role on sites with dry and sandy soils.
Further, ground disturbance is more influential immediately after a
disturbance, but lessens in its importance as succession progresses.
These effects also are more pronounced on the drier sandy sites.
Interactions between gap position and disturbance have more
influence on species evenness and diversity than richness, but
these effects are also site specific. Our results support the idea that
following a disturbance habitat heterogeneity and niche differentiation may be as or more important than overall site productivity in
influencing species richness (Shmida and Wilson, 1985), at least at
small spatial scales.
Temporal factors must also be considered. Understory response
to harvesting consists of the initial effects of the disturbance itself,
and long-term effects resulting from successional change (Roberts
and Gilliam, 2003). Our results from the mesic site show Shannon
diversity and richness initially driven by ground disturbance, but
as succession progressed the influence of gap position became
more prominent. Environmental variation within gaps decreases
with succession, and species cover and composition adjust temporally with these changes (Moore and Vankat, 1986; Collins and
Pickett, 1988; Goldblum, 1997; Ford et al., 2000).
Previous work on till soils found light to be the primary influence on tree sapling growth and not moisture (Pacala et al.,
1994). Ashton and Larson (1996) found that height growth for
oak seedlings is greatest in gap centers of valley positions in comparison to drier ridges, suggesting moisture does play a role. Our
results show richness in the two moister sites already beginning
to decrease within 10 years of gap creation, while richness in the
drier sandy sites is still increasing. This implies that competition
from the regenerating stand has usurped light resources within
10 years on the better sites, while the sandy sites still have ample
available growing space. The relationship between certain guilds
(e.g., ruderal species) and known patterns of establishment within
gaps over time suggests that gap effects may be short-lived (Fahey
and Puettmann, 2008). In fact, Beaudet et al. (2004) found that
shade levels returned to pre-disturbance levels after just 13 years.
Our data shows overall higher establishment and height growth of
seedlings on the mesic and mid-slope sites, particularly within the
M.C. Duguid et al. / Forest Ecology and Management 303 (2013) 148–159
lethal treatments (Frey, 2012). The role of succession is also
evident in the interaction plots (Fig. 5). The mesic site, which has
faster sapling growth, has more divergent interactions in 2004,
becoming insignificant by 2010. The sandy-skeletal site shows a
lag behind the mesic, becoming more divergent as time goes on.
We only examined effects 10 years after gap-creation. It would
be useful to revisit after a longer temporal scale to further elucidate the difference in successional time frame amongst sites.
Across the four sites we see a positive correlation between species richness and site productivity before gap creation (Grime,
1973; Grace, 1999; Mittelbach et al., 2001), though the response
to disturbance is not equal across sites. By 2010, jackknife estimates indicate the sandy-skeletal site almost quadrupled in richness while still trending upward, while the mesic site had only
doubled at its peak. One explanation is pre-disturbance composition and species life-history traits, which play an important role
in determining post-disturbance communities (Halpern, 1989; Aikens et al., 2007). In a compositional study on the mid-slope site,
Aikens et al. (2007) found that although species composition changed in both lethal and release treatments, the release treatments
more closely resembled pre-disturbance communities. Gap centers
were dominated by early successional species, while edge plots
were dominated by residual species (and did not differ between
the north and south edge). We did not analyze species compositional change, but the compositional pattern Aikens et al. (2007)
observed in the mid-slope location did hold true for diversity as
well. Whether compositional diversity follows the same pattern
as species diversity across the other sites is not clear. The importance of compositional diversity to ecosystem function is becoming
increasingly clear (Diaz and Cabido, 2001). Further research is
needed that incorporates the role of life history traits in determining response to disturbance. More research is also needed to evaluate whether compositional and functional diversity is maximized
under the same conditions as species diversity.
157
ment. Managers should not necessarily avoid all soil disturbance
during harvesting operations, but encourage an intimate mixture
of site preparation treatments where scarification is done adjacent
to protection of the understory. One way would be to combine protected areas that may have advance regeneration, and scarifying
areas where there is no regeneration present. In selection treatments, larger irregular gaps with increased edge provide more habitat opportunities for a variety of species. The orientation of the gap
is also important. When possible, gaps should be oriented so species of high conservation value can be maintained on south sides
of gaps, and care should be taken to minimize harsh north edges
that can contribute to dominance by aggressive colonizing species.
Acknowledgements
The Mellon Foundation and the Leopold Schepp Foundation
funded this research. The authors would like to thank Yale-Myers
Forest and The University of Massachusetts for infrastructure and
logistical support. We are grateful to John McKenna, Melissa Aikens, Eli Sagor, Avril de la Cretaz, Caroline Kuebler, Samantha Rothman, Fulton Rockwell, and Jason Nerenberg for data collection and
fieldwork. Thank you to Elaine Hooper, Stella Cousins, Kristofer
Covey, Jeff Carroll, Karin Burghardt, the Silviculture & LMS labs at
Yale School of Forestry and Environmental Studies for support
and feedback during the preparation of this manuscript, and to
two anonymous referees for their comments and feedback on earlier drafts.
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.2013.04.
018.
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