Individual and interactive effects of white-tailed deer and an exotic shrub on artificial and natural regeneration in mixed hardwood forests
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Individual and interactive effects of white-tailed deer and an exotic shrub on artificial and natural regeneration in mixed hardwood forests
Charlotte F. Owings 1
Douglass F. Jacobs 1
Joshua M. Shields 0
Michael R. Saunders 1
Michael A. Jenkins 1
Guest Editor: David Gorchov
0 Manistee Conservation District , 8840 Chippewa Highway, Bear Lake, MI 49614 , USA
1 Department of Forestry and Natural Resources, Purdue University , 715 West State Street, West Lafayette, IN 47906 , USA
Underplanting tree seedlings in areas where natural regeneration is limited may offer a tool by which desired overstory composition can be maintained or restored in forests. However, invasive plant species and ungulate browsing may limit the effectiveness of underplanting, and in-turn, the successful restoration of forest ecosystems. Individually, the invasive shrub Lonicera maackii and browsing by white-tailed deer (Odocoileus virginianus) have been found to negatively affect the regeneration of native tree species in the Midwestern United States, but few studies have examined their interactive or cumulative effects. Using exclosures and shrub removal at five sites, we examined the effects of white-tailed deer and L. maackii both on underplanted seedlings of Castanea dentata and Quercus rubra and on the composition, species richness and diversity of naturally regenerated native tree seedlings. Individually, both deer and L. maackii had negative effects on the survival of underplanted seedlings, but we identified no interactive effects. The presence of L. maackii or deer alone resulted in similar declines in the survivorship of Q. rubra seedlings, but the presence of deer alone resulted in lower survival of C. dentata seedlings than the presence of L. maackii alone. Lonicera maackii reduced light levels, increased seedling moisture stress and decreased relative basal diameter growth for Q. rubra seedlings. Deer reduced the relative growth in height of underplanted C. dentata and Q. rubra seedlings and increased moisture stress of C. dentata seedlings. No effects of L. maackii or deer were found on soil or foliar nitrogen or the overall abundance, species richness and diversity of naturally regenerated seedlings. However, L. maackii and white-tailed deer did affect the abundance of individual tree species, shifting composition of the regeneration layer towards shade tolerant and unpalatable and/or browse tolerant species.
Ecological restoration; field experiment; forest development; herbivory; invasive plants; moisture stress; natural and artificial regeneration; ungulates
Successful regeneration of overstory species is integral
to maintaining forest systems in a time of ecological
(Reyer et al. 2015)
. However, overabundant
ungulate populations and the spread of invasive plants
pose a threat to the regeneration of ecologically and
economically valuable native tree species in many parts
of the world
(Coomes et al. 2003; Vavra et al. 2007;
Jacobs et al. 2015)
. The negative effects of ungulates
and invasive plants are typically more pronounced in
fragmented landscapes, where forests exist as small
patches within a matrix of agriculture and exurban
(Minor et al. 2009; Hurley et al. 2012)
North America, the Midwestern United States offers an
archetype of a fragmented landscape altered by invasive
(Luken 1997; Oswalt et al. 2015)
and a frequently
overabundant ungulate species
Anderson 1997; Hurley et al. 2012)
In the last century, white-tailed deer abundance has
increased as a result of reduced predation, greater
forage from agriculture and tree plantings and increased
(C oˆte´ et al. 2004)
. White-tailed deer
preferentially browse certain species, altering forest dynamics
over time by shifting composition towards species that
are unpalatable or browse-tolerant
(Rooney and Waller
2003; Rossell et al. 2005)
. White-tailed deer alter nutrient
cycling by preferentially browsing plants that have
nutrient-rich tissue, over time, increasing the abundance
of nutrient-poor species which decompose more slowly
(Ritchie et al. 1998; C oˆte´ et al. 2004)
. White-tailed deer
alter nitrogen cycling by increasing the amount of
available nitrogen in the soil through faeces and urine and by
altering plant composition, and thus litter quality,
(Hobbs 1996; Ritchie et al. 1998;
Murray et al. 2013)
. Ultimately, composition and
structure of forests are altered as heavily browsed species
such as oak (Quercus spp.) are lost, and the regeneration
layer is dominated by less-preferred or browse-tolerant
species such as Fraxinus americana or Prunus serotina
(Tilghman 1989; Rossell et al. 2005)
In addition to ungulates, natural regeneration of
native tree seedlings can be limited by competition with
other species, in particular invasive plants. Amongst
invasive plants species, shrubs are often the most
problematic in forests because they form thick understory
layers that are alien structural elements in many forests
and overtop woody seedlings
(Merriam and Feil 2002;
Webster et al. 2006; Shields et al. 2015a)
. For example,
one species of invasive shrub that limits the natural
regeneration of native tree seedlings is Lonicera maackii
(Hutchinson and Vankat 1997; Collier et al. 2002;
Gorchov and Trisel 2003 Shields et al. 2015b)
, which was
first cultivated in the United States in the late 1800s and
has now spread to 28 states
(Luken and Thieret 1994;
USDA, NRCS 2015)
. Lonicera maackii is a superior
competitor to many native species, grows rapidly, has
extensive roots near the soil surface that facilitate the uptake
of nutrients and water, and possesses an extended leaf
phenology compared with native species
Gorchov 2000; Hutchinson and Vankat 1997; McEwan
et al. 2010; Pfeiffer and Gorchov 2015)
. In addition, L.
maackii has been found to alter nutrient cycling in
invaded areas through accelerated release of litter N
resulting from a lower C:N ratio and more rapid litter
decomposition than native species
(Blair and Stowasser
2009; Poulette and Arthur 2012; Schuster and Dukes
. These alterations could align the release of
nitrogen with the expanded growing season of invasive
shrubs such as L. maackii, potentially furthering its
(Blair and Stowasser 2009; Schuster
and Dukes 2014)
Quercus rubra and Castanea dentata are two
economically and ecologically valuable tree species that have
limited natural regeneration across their extensive
historic range in eastern North America. Quercus rubra has
experienced widespread regeneration failure as a result of
(Brose et al. 2014)
and herbivory by
overabundant populations of white-tailed deer
(Buckley et al.
1998; Castleberry et al. 1999; Rooney and Waller 2003)
resulting in drastic increases in the dominance of
shadeand browse-tolerant mesophytic species in forest
(Abrams 1992; Brose et al. 2001, 2014)
dentata has largely disappeared from its historically
extensive range as the result of chestnut blight
(Cryphonectria parasitica), a pathogen introduced in the
. The loss of this foundation
species spurred research efforts to develop a
blightresistant hybrid though backcross breeding with
Castanea mollissima, an Asian species
(Jacobs et al.
. The resulting seedlings are primarily C. dentata
genetically (>90 %) and may offer an opportunity to
restore C. dentata to native forests as restoration
prescriptions are developed
(Burnham 1986; Diskin et al. 2006;
Jacobs et al. 2013)
In the long-term, restoring degraded forests in
fragmented landscapes may depend upon artificial
regeneration techniques, such as underplanting, to increase the
importance of desired species in hardwood forests
et al. 2012)
. Underplanting can reduce the amount of
site preparation necessary for restoration, thus
decreasing the amount of resources needed to restore forested
(Belair et al. 2014)
. Underplanting can be used in
areas with low abundance of natural regeneration and
may allow management to function on controlled time
scales as the technique does not require the long process
VC The Authors 2017
of fostering natural regeneration
(Loftis 1990; Paquette
et al. 2006)
. For species such as Q. rubra, seedling growth
is optimized under partial canopy (often created by
shelterwood harvest) and the underplanting of seedlings can
provide advanced regeneration before initial openings
. Recent work has shown that
the growth of C. dentata seedlings exhibit a similar
response to partial canopy removal and outperform other
species, including Q. rubra, when underplanted
et al. 2014)
. While underplanting is a useful restoration
tool, obstacles such as herbivory from wildlife and
competition from other species may reduce the successful
establishment and growth of underplanted seedlings
(Dey et al. 2012).
While the impacts of L. maackii and white-tailed deer
on native tree seedlings have been studied individually,
less is known about their combined effects. Lonicera
maackii in the understory could help to physically protect
tree seedlings from deer browsing by providing cover, but
may also create a microenvironment that inhibits the
germination, establishment, growth and survival of
Aronson and Handel (2011)
management of invasive plants and white-tailed deer
may be necessary for the natural regeneration of native
canopy trees to persist. In a study of the effects of
honeysuckle and white-tailed deer on the survival of sugar
Loomis et al. (2015)
found that, individually,
both honeysuckle and white-tailed deer negatively
affected seedling survival, but no significant interaction
between the two factors was found. Active management
methods, such as underplanting, protecting planted tree
seedlings from herbivory and removing invasive shrubs
may be necessary to restore forested areas in which both
invasive shrub species and white-tailed deer are present.
In this study, our objectives were to examine the
individual and combined impacts of L. maackii and
whitetailed deer on underplanted Q. rubra and C. dentata
seedlings, as well as on the composition of naturally
regenerated seedlings of woody species. We conducted
our study in five forests within the glaciated till plain of
IN, USA (Table 1). Typical of the Midwest region, forests
in this area largely consist of small fragments within an
agricultural matrix. Deer hunting occurred on three of
our sites and in the matrix surrounding the remaining
two sites. We did not observe evidence of heavy deer
(browse lines, lack of native woody understory in
areas without dense L. maackii, extirpation of lily species;
Waller and Alverson 1997)
at any of our sites. For our
study design, we utilized two treatments: deer exclusion
and honeysuckle removal.
We hypothesized that white-tailed deer and L. maackii
would collectively have more negative impacts on forest
seedlings than either treatment alone. However, when
both treatments were considered individually, we further
hypothesized that L. maackii would have a greater
suppressive effect on seedlings than deer, but would also
mitigate the direct effects of deer. Specifically, due to
above and below competition created by high stem
densities of L. maackii in invaded sites, we predicted
(i) growth, survival and foliar nitrogen content of
underplanted seedlings would be lower and water stress
higher in the presence of L. maackii alone than in the
presence of deer alone. However, we predicted that
(ii) the rate of browsing of underplanted seedlings
outside of the exclosures would be lower under the
protective cover of L. maackii. We also predicted that (iii) acute
competition created by the presence of L. maackii alone
would result in lower abundance, richness and diversity
of naturally regenerated seedlings than in the presence
of deer alone.
This study was conducted at five sites within the
glaciated region of IN, USA: (i) Martell Experimental Research
Forest (Martell); (ii) Vigo County Park District property
(Terre Haute); (iii) Ross Biological Reserve (Ross);
(iv) Purdue University Department of Forestry and
Natural Resources Lugar Farm (Lugar Farm) and (v) a
privately owned woodlot (Pursell; Table 1). Sites were within
mature secondary deciduous forests that were heavily
invaded by L. maackii and in which L. maackii was the
dominant invasive species
(Shields et al. 2015a)
. The age
and level of L. maackii invasion, soil type and overstory
composition varied across the five sites (Table 1).
Two 80 80 m areas were designated at each of the
five study sites. In one 80 80 m area, all woody invasive
plant species were removed between November 2010
and March 2011 at four sites (Terre Haute, Ross, Lugar
Farm and Pursell) and in February 2013 at the remaining
site (Martell). The second 80 80 m area was untreated
and served as a reference area
(Shields et al. 2015b)
Lonicera maackii was removed by either cutting the
shrub at the base using a brush saw or loppers and
treating the stump with herbicide (20 % Garlon 4 VR triclopyr,
1 % Stalker VR imazapyr and 79 % Ax-it VR basal oil), or by
manually pulling small shrubs (single stems < 80 cm
height) out of the ground
(Shields et al. 2015b)
cutting, large shrubs were then removed from the site. New
and re-sprouted shrubs were re-treated by cutting and
applying herbicide on the cut surface in the summer of
2014 to maintain the removal areas.
In the spring of 2013, two 20 40 m units were
established in each 80 80 m removal and reference area.
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Study site Lat/long Annual Dominant overstory species Soils Invasion L. maackii Deer
precip. age density visits
(cm/yr) (years) (stems/ha)
Lugar Farm 40 250N 86 570W 97.03 Robinia pseudoacacia, Juglans nigra Silt loams 35 3135 6 863 19
One of the two units was randomly selected as a deer
exclosure area and a 2.5-m tall fence was constructed
around the exterior to prevent white-tailed deer from
accessing the unit. Small mammals, however, were able to
enter the exclosure beneath the fence. Fences were
checked periodically for damage and repaired as
necessary. No fence was constructed around the second
20 40 m unit, allowing deer to access these areas.
After fence construction, each study site contained four
treatment combinations: (i) L. maackii removed and
accessible to deer, (ii) L. maackii removed and deer
excluded, (iii) L. maackii present and accessible to deer and
(iv) L. maackii present and deer excluded.
A severe windstorm on 17 November 2013 resulted in
heavy damage to the removal area at the Lugar Farm
site. The storm resulted in windthrow of over half the
forest canopy, resulting in increased light availability and
large inputs of woody debris. Debris was cut and removed
from around the planted seedlings and natural
regeneration transects in the two removal subunits to allow deer
access comparable to the pre-storm condition. In the
reference area, which was largely undamaged, selected
trees were girdled in the spring of 2014 in order to create
similar openings in the canopy to those in the removal
areas while preserving the dense L. maackii shrub cover.
Tree seedling study species and underplanting
Each treatment unit was divided length-wise into two
sections. One of the sections was randomly assigned for
tree seedling planting and the other was assigned for the
sampling of natural regeneration. For planting, we
obtained 800 one-year-old bareroot Q. rubra and C. dentata
seedlings that were produced according to standard
operational nursery practices
State Tree Nursery in southern Indiana. Twenty seedlings
of each species were planted by hand in two lines spaced
2 m apart in each study unit in April of 2014. Within lines,
the two species were randomly mixed and seedlings
were planted 1.5 m apart. To allow establishment,
competing vegetation was removed by hand within a meter
of each seedling at the beginning of the study.
Seedling characteristics and browse
Survival, height and basal diameter (to the nearest
0.01 mm) were measured for each seedling at the
beginning and end of the growing season. The presence of
deer and rabbit browse was also recorded. Rabbit browse
was distinguished from deer browse by examining the
browsed area on the stem of the underplanted seedling.
Rabbit browsed seedlings had clean and angled cuts
while seedlings browsed by deer were more scraped and
jagged in appearance. To confirm the presence of deer at
each of the sites, two trail cameras (HC600 Hyperfire,
RECONYX, Inc., Holmen, WI, USA) were placed in the two
non-exclosure (removal and reference outside) subunits
at each of the study sites during June and September
2014 and images were examined for deer. Total deer
visits ranged from 19 at Lugar Farm to 86 at Ross (Table 1).
VC The Authors 2017
Seedling moisture stress and foliar nutrient concentration
Pre-dawn plant moisture stress was measured for five
randomly selected seedlings per species from each of
the units during 12–15 August 2014. One leaf was
collected from each seedling at approximately the same
location along the stem and the leaf xylem water potential
was determined using a pressure chamber
PMS Instruments, Corvallis, OR, USA; Waring and Cleary
After moisture stress measurements were taken,
collected leaves were dried at 65 C for 48 h. The dried
samples were then ground in a ball mill. Foliar N
concentration was determined for each foliar sample
using an elemental analyzer (ECS 400, Costech Analytical
Technologies, Inc., Valencia, CA, USA).
Light measurements and soil N availability
To determine the amount of photosynthetically active
radiation (PAR) in each study unit, PAR measurements
were taken using a light ceptometer (LP-80 AccuPAR
Ceptometer, Decagon Devices, Inc., Pullman, WA, USA) in
July 2015. All measurements were made 1 m above
the ground on cloudless days between 1 h prior and 1 h
after solar noon. PAR measurements were taken in an
open field adjacent to each study site to determine the
(Grayson et al. 2012)
. Within the study
units, PAR readings were taken above every fifth
Twelve soil subsamples from 0 to 20 cm depth were
collected from each of the four treatment subunits using
a soil probe. Four composite samples were formed by
pooling three soil samples randomly chosen from the
same subunit. Samples were refrigerated and then sent
to Brookside Laboratories, Inc. (New Bremen, OH, USA)
and tested for total nitrogen
(NO3 and NH4; Nelson and
Sommers 1996; McGeehan and Naylor 1988)
Natural tree regeneration
In the section of the treatment unit assigned to natural
regeneration, three 10 m-long permanent transects were
established with each transect spaced a minimum of
5 m from the next nearest transect. Five 1 m2 quadrats
were placed every other meter along the right side of
each 10 m transect. Woody stems <50 cm in height
were tallied by species within the 1-m2 quadrats during
late July/early August 2013, 2014 and 2015. The stem
and species tallies were used to determine the density,
species richness and species diversity of naturally
regenerating woody stems for each unit. Woody vines were
not included in the tally.
Calculations and statistical analyses
For each underplanted seedling, relative changes in
height and basal diameter were calculated by
determining the change in height and basal diameter over the
course of the growing season (height/basal diameter in
fall – height/basal diameter in spring) and dividing this
value by the initial height and initial basal diameter,
respectively. For the relative change in height and basal
diameter analyses, dead trees were excluded. Negative
values of relative growth in basal diameter were
excluded from analyses as likely being a reflection of dead
seedlings. Relative changes in growth data (height and
basal diameter) were transformed using an arcsine
square root transformation to improve normality.
Percent ambient PAR was calculated by dividing the PAR
value recorded above every fifth seedling by the average
ambient PAR value from 15 readings
(Grayson et al.
. These values were log-transformed to improve
normality for statistical analyses. The species richness,
evenness and diversity of naturally regenerating
seedlings were calculated from the natural regeneration
quadrat data. Species richness was calculated as the
number of unique species per transect and species
diversity was calculated using the Shannon Diversity Index.
Species diversity, evenness and richness were
calculated using the software PC-ORD 5
(McCune and Mefford
. Species within the same genus were grouped
together for analysis because many individual species did
not occur across all study sites. These groupings included
Carya spp., Quercus spp. and Ulmus spp.
All statistical analyses were performed using R
(R Core Team 2013)
and significance was
determined at a ¼ 0.05. The R statistical packages
‘survival’ and ‘coxme’
were used to
determine the fixed effects of L. maackii, white-tailed deer,
their interaction, and the random effect of site on the
survival of the underplanted C. dentata and Q. rubra
seedlings. The ‘coxme’ and ‘survival’ packages were used
to analyse survival using a Cox proportional hazards
model to determine differences in the relative risk of
mortality amongst treatments from the beginning to the
end of the study.
Generalized linear mixed effects models were
performed using the R package ‘lme4’
(Bates et al. 2015)
determine the fixed effects of L. maackii, white-tailed
deer, their interaction, and the random effect of study
site on foliar and soil nitrogen concentration, moisture
stress, browse, natural regeneration, PAR and
underplanted seedling growth (basal diameter and height).
Time (year of measurement) was also included as a
factor in the natural regeneration analyses as these data
represented changes across three years
(2013, 2014 and
while the data for the underplanted seedlings
VC The Authors 2017
represented change over one year or one time point of
measurement. Each site was considered as a replicate in
our analyses. A Poisson distribution was used to model
natural regeneration density, an inverse Gaussian
distribution was used to model moisture stress, and all other
measurements were modelled using a normal
distribution. Data from Ross were excluded from the plant
moisture stress and foliar N analyses as one of the
treatments had no trees with foliar tissue to measure.
However, we were still able to compare plant moisture
stress and foliar N across all four treatments at the other
four sites (Farm, Martell, Pursell and Terre Haute).
Because of the large number of statistical tests
performed in our comparisons of natural regeneration
density by species, we adjusted P-values
with a graphically-sharpened procedure based on
control of the false discovery rate
(FDR; Benjamini and
Hochberg 1995, 2000)
. In recent years, multiple
comparison techniques based upon FDR have been used more
frequently in ecological experiments as an alternative to
traditional controls of family-wise error rate because
FDR-based techniques retain statistical power while
keeping the proportion of false discoveries small relative
to all significant results
(Verhoeven et al. 2005; Pike
Survival of underplanted seedlings
Supporting our hypothesis, the greatest survival for both
species was in the treatment combination where
L. maackii was removed and deer were excluded, while
the lowest survival for both species was in the reference
areas outside of the exclosures where only 10 % of
seedlings survived after two growing seasons (Fig. 1,
Table 2). There was no significant interaction between
L. maackii and white-tailed deer for the survival of either
species. For C. dentata, the second highest survival rate
was in areas in which L. maackii was present and deer
were excluded, countering our prediction that L. maackii
alone would have a greater impact on survival than deer
alone. Lonicera maackii removal areas outside the
exclosures exhibited the next lowest survival rate. For Q. rubra,
survival did not differ between the treatment in which
L. maackii was present inside the exclosures and where it
was removed outside the exclosures (Fig. 1).
Seedling characteristics and browse
The presence or absence of L. maackii outside of the deer
exclosures did not significantly impact the number of
underplanted seedlings of either species browsed by the
end of the study, a finding that did not support our
prediction that L. maackii would protect seedlings from
browsing (Table 2). We observed a significant difference
in relative height during the first growing season, with
white-tailed deer having a negative effect on growth in
height for seedlings of both species (Fig. 2, Table 2).
While L. maackii did not have a significant effect on
height for Q. rubra, there was a significant interaction
between L. maackii and deer on height for C. dentata, with
greater height growth in the treatment without
L. maackii and deer (Table 2), supporting our prediction
that seedlings would grow best when deer and L. maackii
were absent. However, the next greatest height growth
occurred in the treatment with L. maackii and without
deer (Fig. 2, Table 2) and the least growth in height for
C. dentata occurred in the two treatments in which deer
had access (Fig. 2, Table 2), countering our prediction
that L. maackii would have greater effects on height
growth than deer.
Deer did not have an effect on growth in basal diameter
for either underplanted species. There was no difference
amongst treatments in relative change in basal diameter
VC The Authors 2017
for C. dentata (Fig. 3). For Q. rubra, relative change in basal
diameter was greater in the areas where L. maackii was
present (Fig. 3). The high mortality of seedlings in some of
the treatments during the second growing season did not
allow us to examine changes in basal diameter or height
over the second growing season.
VC The Authors 2017
Seedling moisture stress, PAR, and foliar and soil N
Plant moisture stress was greater where L. maackii was
present for both species of underplanted seedlings and
outside the exclosures (deer present) for C. dentata (Fig.
4; Table 2). Percent ambient PAR was lower in areas in
which L. maackii was present compared with where it
was removed (Table 3). There was no difference in PAR
between the exclosed and unexclosed areas within the
L. maackii removal and reference areas (Tables 2 and 3).
No significant difference was found in foliar nitrogen
concentration amongst the treatments for either the Q.
rubra or C. dentata underplanted seedlings (Table 2).
There was also no significant differences in soil nitrogen
amongst the treatments (Tables 2 and 3).
Contrary to our predictions, neither the presence of L.
maackii nor white-tailed deer had an effect on the overall
density of native tree seedlings across treatments. There
was also no effect of L. maackii or white-tailed deer on
the species richness, evenness, or diversity of naturally
regenerated tree seedlings (Table 4). No invasive tree
seedlings were encountered in our units.
Amongst individual species, the density of Acer
saccharum, a highly shade-tolerant species, was greater
where L. maackii was present than where it was removed
(Tables 4 and 5, while the density of P. serotina was
greater in the areas where L. maackii was removed
(Table 5). Regardless of treatment, the density of P.
serotina decreased over time. There was a significant
interaction of L. maackii and time on the density of
F. americana, with F. americana density decreasing over
time in the L. maackii reference areas, but increasing in
the removal areas. In contrast, the densities of F.
americana and Ulmus spp. increased significantly outside of
the exclosures over the course of the study and declined
inside. The only significant interaction between
whitetailed deer and L. maackii was for the density of Ulmus
spp., which was greater in the treatment with L. maackii
and white-tailed deer and did not differ amongst the
other three treatments (Table 4).
VC The Authors 2017
Survival and growth of underplanted seedlings
Our finding that the presence of L. maackii and deer
resulted in the lowest survival of underplanted seedlings of
C. dentata and Q. rubra supported our hypothesis and
the results of other studies that examined the individual
effects of L. maackii and white-tailed deer and found
each to have negative effects on the survival of naturally
regenerating native tree seedlings
(Loomis et al. 2015;
Gorchov and Trisel 2003; Rossell et al. 2005)
increased survival of underplanted seedlings in areas in
which L. maackii was removed and white-tailed deer
excluded is likely due to a number of factors. In our study,
percent ambient PAR was lower in the areas in which L.
maackii was present. Both Q. rubra and C. dentata
seedlings have intermediate tolerance of shade, but are
intolerant of heavy shade
(Crow 1988; Joesting et al. 2009)
Thus, the reduced light levels in the L. maackii reference
areas may have contributed to lower survival of the
underplanted seedlings in the heavily shaded reference
areas. Furthermore, reducing midstory basal area can
promote growth and establishment of Q. rubra and C.
(Loftis 1990; Brown et al. 2014)
removal of L. maackii in our study may have had a similar
effect resulting in increased light availability to the
underplanted seedlings, especially at sites with high
preremoval densities of mature L. maackii (Table 1).
Overall, our results illustrated that, contrary to our
prediction, the negative individual effects of deer on survival
and height growth of underplanted seedlings were
greater than those of L. maackii. One of the mechanisms
by which white-tailed deer may have reduced survival of
the underplanted seedlings is by reducing seedling
height and photosynthetic tissue through browse. Other
studies have found that height of naturally regenerating
seedlings is greater in areas in which deer have been
excluded or in areas with lower deer abundance
et al. 2003; Aronson and Handel 2011; Shelton et al.
Gorchov and Trisel (2003)
proposed that L.
maackii may deter browsing of native seedlings by
white-tailed deer. However, contrary to our prediction,
we did not find a difference in the percent of
underplanted seedlings browsed in non-exclosure areas by the
end of the study. However, relative growth in height was
greater with the exclusion of deer for both species of
underplanted seedling, indicating that there was a negative
effect of browsing on underplanted seedling growth. We
observed no effect of L. maackii on relative growth in
height for Q. rubra, but did find an interactive effect of L.
maackii and deer on C. dentata, with underplanted
seedling height being greatest where both were removed
followed by where honeysuckle was present, but deer were
excluded, indicating a stronger negative effect of deer.
An effect of L. maackii on basal diameter was found for
Q. rubra underplanted seedlings, with greater growth in
areas in which L. maackii was removed. This finding may
be a result of the higher PAR in the removal areas
allowing for greater growth.
The lower survival of the underplanted seedlings in
areas with deer and L. maackii may have been, in part, a
result of increased seedling moisture stress in our study.
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Moisture stress of the underplanted seedlings was
greater in the areas in which L. maackii was present for
both species of underplanted seedlings, and for C.
dentata, was greater in the areas accessible to deer. We
predicted that moisture stress would be greater in areas
with L. maackii, which reduces soil moisture and
throughfall, potentially resulting in less water available
(Pfeiffer and Gorchov 2015)
during the two weeks prior to our measurements was
almost twice the normal amount
(U.S. Climate Data 2015)
potentially having an impact on our results as
underplanted seedlings may not have been under as high of
stress as that which may typically occur under drier
conditions. Despite this increased rainfall, we still detected
differences in moisture stress, suggesting that deer may
be increasing moisture stress of the underplanted
seedlings through herbivory. The increased moisture stress
created by the presence of L. maackii and deer likely has
a stronger effect on mortality and growth during the
periodic meteorological droughts that occur in the
Midwestern United States
(Mallya et al. 2013)
Contrary to our predictions, neither L. maackii nor
whitetailed deer had a significant effect on the overall density,
richness or diversity of naturally regenerating native
seedlings. In contrast, other studies have found reduced
Table 5 Density (stems/hectare 6 1 SE) of native tree seedlings
across sites averaged across sampling periods from fall 2013 to
2015 in the treatments where L. maackii was present (L. maackii)
and removed (no L. maackii). Superscript letters next to the species
represent significant interactions between L. maackii and time (T)
and deer (D). P-values for density were adjusted for multiple
comparisons with a graphically sharpened procedure to control the
false discovery rate
(Benjamini and Hochberg 1995)
Species L. maackii No L. maackii P-value
Acer saccharum 8960 6 1940 640 6 200 0.005
native tree seedling density, richness, diversity and
survival under L. maackii
(Collier et al. 2002)
and in areas in
which white-tailed deer are present
Rossell et al. 2005; Aronson and Handel 2011;
VC The Authors 2017
Frerker et al. 2014)
. While both L. maackii and
whitetailed deer can individually have negative effects on
native tree seedling survival and density,
Gorchov and Trisel
suggested that there may be an interaction
between L. maackii and white-tailed deer in which
L. maackii protects seedlings from browse and increases
their survival. However, we found no interactive effect of
white-tailed deer and L. maackii on overall seedling
density, richness or diversity in our study.
The short time period in which our exclosures were in
place may not have allowed us to detect changes in
overall density and diversity resulting from deer
herbivory. While L. maackii was removed from the sites up to
three years prior to the beginning of the study, deer had
only been excluded for 2.5 years by the end of the
study. While changes in herbaceous-layer diversity
richness and diversity have been found to occur quickly
(1 year) after L. maackii removal
(Shields et al. 2015b)
changes in the herbaceous layer following deer exclusion
may take longer to manifest (10þ years) and may not be
detectable over shorter periods
(Griggs et al. 2006;
Collard et al. 2010; Frerker et al. 2014; Waller 2014)
addition, while deer population densities in our study
areas were likely representative of densities across much
of the Midwest, our sites do not have the long history of
heavy overabundance documented in studies from other
(Horsley et al. 2003; Griggs et al. 2006)
Therefore, changes across our sites following deer
exclusion may be subtler and slower to develop. However, the
high rate of browse on the underplanted seedlings in our
study shows that deer are affecting regeneration.
Furthermore, the contemporary regeneration layer of
forests across the Midwest reflects the cumulative
effects of a regional deer population that is likely in excess
of historic levels (Coˆte´ et al. 2004).
Other studies have observed suppressed regeneration
as a result of lower light
(Luken and Thieret 1994)
(Dorning and Cippollini 2006)
, and reduced soil
(Pfeiffer and Gorchov 2015)
beneath L. maackii.
In our study, the areas in which L. maackii was removed
experienced large increases in the cover and height of
herbaceous species (Freeman 2015), which may have
reduced the survival of naturally regenerated seedlings
through intensified competition as has been observed
with natural regeneration of pine species
(Cain 1991; Pitt
et al. 2009, 2010)
While there was no effect of L. maackii or white-tailed
deer on total native seedling density, richness or
diversity, density and relative density differed for individual
species and groups. Prunus serotina density was greater
where L. maackii was removed, while A. saccharum
density was lower in the absence of L. maackii. Shields et al.
(2015b) found increases in P. serotina immediately
following the removal of L. maackii across four of the
sites in this study (our Martell site was not included in
the study). While the high fecundity of this species allows
it to produce high densities of seedlings, they are unlikely
to grow out of the regeneration layer without canopy
disturbance. While A. saccharum in our study may be
able to reproduce under L. maackii cover, we did not
assess the survival of individual seedlings. A recent study
Loomis et al. (2015)
found no difference in A.
saccharum survival after one year between plots where L.
maackii was present and where it was removed,
suggesting that the high shade tolerance of the species may
allow it to persist under L. maackii cover. While we did not
observe significant effects of deer or L. maackii on
seedlings of Quercus species, densities of this genus were low
across our study sites and likely precluded our ability to
Through time, the density of two species groups,
Ulmus spp. and F. americana, decreased inside the
exclosures while increasing outside. While F. americana is
browsed by deer
, the species can
remain abundant in the presence of white-tailed deer and
may be more tolerant of browse than many other tree
species, allowing its density to remain high outside of
(Rossell et al. 2005; Jenkins et al. 2014)
Similar to F. americana, the density of Ulmus spp. was
greater outside the exclosures than inside (Table 4).
Density of this species displayed a significant interaction
between L. maackii and deer, with greater relative
density in the presence of both L. maackii and deer. In areas
of high deer populations, Ulmus spp. can be a frequently
browsed species (Pogge 1967); however, in areas of
lower deer abundance, it may be avoided when other
more palatable species are available
(LaGory et al. 1985;
Sotala and Kirkpatrick 1972)
Tree recruitment is a critical mechanism for the
maintenance of ecological resilience in forests
(Reyer et al.
. However, maintaining successful regeneration of
native forests has become increasingly difficult in this
era of global change. Shifts in the historical abundance
of browsing ungulate populations and spread of invasive
plant species are frequently identified as paramount
challenges to forest regeneration worldwide, particularly
in fragmented landscapes.
As in many other forests, the effects of ungulate
herbivory, invasive plants and altered disturbance regimes
were highly evident across our study sites. We observed
natural regeneration layers that were dominated by late
seral and browse tolerant species. The presence of
VC The Authors 2017
L. maackii favoured only the most shade tolerant species
(A. saccharum) and the added effects of deer pushed
seedling-layer composition towards F. americana and
Ulmus spp. However, F. americana and Ulmus spp. are
unlikely to persist in the future canopy of these forests
due to the effects of introduced insects and disease
(Lovett et al. 2016)
. Under these conditions of
depauperate natural regeneration, underplanting offers a
potential, albeit expensive, technique to begin the restoration
of desired species to degraded forests. Our study found
that the removal of L. maackii increased understory light
levels in a way similar to a technique offered by
to regenerate oak species on mesic sites. This
technique mechanically reduces the density of the
midstory to increase light levels and foster the survival and
growth of advance regeneration, which is ultimately
released when canopy openings are created. Using a
similar sequence, L. maackii removal, in conjunction with
underplanting, could be a first step in restoring degraded
hardwood forests. However, our results showed that the
presence of deer had a greater negative effect on the
survivorship of C. dentata seedlings than shading by L.
maackii. The low survival of both underplanted species in
the presence of deer and L. maackii demonstrates that
both deer and L. maackii must be managed if restoration
efforts are to be successful.
Sources of Funding
This research was supported with funds from the
Department of Forestry and Natural Resources and the
Hardwood Tree Improvement and Regeneration Center
at Purdue University and the USDA McIntire-Stennis
Cooperative Forestry Program (project IND011533MS).
Contributions by the Authors
This article was derived from the MS thesis of C.F.O., who
was co-advised by D.F.J. and M.A.J. Study design was a
collaborative effort of D.F.J., J.M.S., M.R.S. and M.A.J.
C.F.O. performed the analyses and led the writing effort.
D.F.J. and M.A.J. contributed text and all authors edited
Conflicts of Interest Statement
We thank Lindsay Keitzer, Brad Graham, Patrick Duffy,
Rob Quackenbush, Jenny Lesko, Kyle Earnshaw, Mike
Szuter, Mercedes Uscola, Safi Khurram, Carmen Dobbs,
Joe Littiken, Keeli Curtis, Allison Hyrcik, Heather Pasley,
Josh Sloan and Taylor Owings for their help with various
aspects of this project. We also thank Bryan Murray,
Nathan Lichti and Rongong Zhang for their assistance
with statistics, Sally Weeks for her help with species
identification, and Tim Smyser, Liz Flaherty and Mike
Saunders for their assistance with the Reconyx cameras.
We thank Brian Beheler and Michael Loesch-Fries for
their help with the construction and maintenance of
exclosures and for cleaning up one of our sites after a
severe windstorm knocked down over 30 trees. We also
thank Brent Pursell, the Vigo County Park District and the
Purdue University Department of Biological Sciences for
allowing access to their properties and Kevin Gibson and
three anonymous reviewers for their helpful comments
on earlier drafts of this paper.
VC The Authors 2017
VC The Authors 2017
Abrams MD. 1992 . Fire and the development of oak forests - in eastern North America, oak distribution reflects a variety of ecological paths and disturbance conditions . Bioscience 42 : 346 - 353 .
Anderson RC . 1997 . Native pests: the impacts of deer in highly fragmented habitats . In: Schwartz MW, ed. Conservation in highly fragmented landscapes. New York: Chapman and Hall, 117 - 134 .
Aronson MFJ , Handel SN . 2011 . Deer and invasive plant species suppress forest herbaceous communities and canopy tree regeneration . Natural Areas Journal 31 : 400 - 407 .
Bates D , Maechler M , Bolker B , Walker S. 2015 . Fitting linear mixedeffects models using lme4 . Journal of Statistical Software 67 : 1 - 48 .
Belair ED , Saunders MR , Bailey BG . 2014 . Four-year response of underplanted American chestnut (Castanea dentata) and three competitors to midstory removal, root trenching, and weeding treatments in an oak-hickory forest . Forest Ecology and Management 329 : 21 - 29 .
Benjamini Y , Hochberg Y. 1995 . Controlling the false discovery rate - a practical and powerful approach to multiple testing . Journal of the Royal Statistical Society: Series B 57 : 289 - 300 .
Benjamini Y , Hochberg Y. 2000 . On the adaptive control of the false discovery rate in multiple testing with independent statistics . Journal of Educational and Behavioral Statistics 25 : 60 - 83 .
Blair BC , Stowasser A. 2009 . Impact of Lonicera maackii on decomposition rates of native leaf litter in a southwestern Ohio woodland . Ohio Journal of Science 109 : 43 - 48 .
Brose P , Schuler T , Van Lear D , Berst J. 2001 . Bringing fire back: the changing regimes of the Appalachian mixed-oak forests . Journal of Forestry 99 : 30 - 35 .
Brose P , Dey DC , Waldrop TA . 2014 . The fire-oak literature of eastern North America: synthesis and guidelines . Gen. Tech. Rep. NRS-135 . Newton Square, PA: U.S. Department of Agriculture, Forest Service, Northern Research Station, 98p .
Brown CE , Bailey BG , Saunders MR , Jacobs DF . 2014 . Effects of root competition on development of chestnut and oak regeneration following midstory removal . Forestry 87 : 562 - 570 .
Buckley DS , Sharik TL , Isebrands JG . 1998 . Regeneration of northern red oak: positive and negative effects of competitor removal . Ecology 79 : 65 - 78 .
Burnham CR . 1986 . Chestnut hybrids from USDA breeding programs . Journal of the American Chestnut Foundation 1 : 8 - 12 .
Cain MD. 1991 . Woody and herbaceous competition effects on the growth of naturally regenerated loblolly and shortleaf pines through 11 years . New Forests 14 : 107 - 125 .
Castleberry SB , Ford WM , Miller KV , Smith WP . 1999 . White-tailed deer browse preferences in a southern bottomland hardwood forest . Southern Journal of Applied Forestry 23 : 78 - 82 .
Collard A , Lapointe L , Ouellet JP , Crete M , Lussier A , Daigle C , Coˆ te ´ SD. 2010 . Slow responses of understory plants of mapledominated forests to white-tailed deer experimental exclusion . Forest Ecology and Management 260 : 649 - 662 .
Collier MH , Vankat JL , Hughes MR . 2002 . Diminished plant richness and abundance below Lonicera maackii, an invasive shrub . American Midland Naturalist 147 : 60 - 71 .
Coomes DA , Allen RB , Forsyth DM , Lee WG . 2003 . Factors preventing the recovery of New Zealand forests following control of invasive deer . Conservation Biology 17 : 450 - 459 .
Coˆ te´ SD , Rooney TP , Tremblay J , Dussault C , Waller DM . 2004 . Ecological impacts of deer overabundance . Annual Review of Ecology, Evolution, and Systematics 35 : 113 - 147 .
Crow TR . 1988 . Reproductive mode and mechanisms for selfreplacement of northern red oak (Quercus rubra) - a review . Forest Science 34 : 19 - 40 .
Dey DC , Gardiner ES , Schweitzer CJ , Kabrick JM , Jacobs DF . 2012 . Underplanting to sustain future stocking of oak (Quercus) in temperate deciduous forests . New Forests 43 : 955 - 978 .
Diskin M , Steiner KC , Hebard FV . 2006 . Recovery of American chestnut characteristics following hybridization and backcross breeding to restore blight-ravaged Castanea dentata . Forest Ecology and Management 223 : 439 - 447 .
Dorning M , Cipollini D. 2006 . Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects . Plant Ecology 184 : 287 - 296 .
Freeman C. 2015 . Vegetation and underplanting response to Amur honeysuckle invasion and deer herbivory in mixed hardwood forests . Thesis , Purdue University, West Lafayette, IN, USA.
Frerker K , Sabo A , Waller D. 2014 . Long-term regional shifts in plant community composition are largely explained by local deer impact experiments . PLoS ONE 9:e115843; doi:10 .1371/journal. pone. 0115843 .
Gorchov DL , Trisel DE . 2003 . Competitive effects of the invasive shrub, Lonicera maackii (Rupr.) Herder (Caprifoliaceae), on the growth and survival of native tree seedlings . Plant Ecology 166 : 13 - 24 .
Gould AMA , Gorchov DL . 2000 . Effects of the exotic invasive shrub Lonicera maackii on the survival and fecundity of three species of native annuals . American Midland Naturalist 144 : 36 - 50 .
Grayson SF , Buckley DS , Henning JG , Schweitzer CJ , Gottschalk KW , Loftis DL . 2012 . Understory light regimes following silvicultural treatments in central hardwood forests in Kentucky, USA . Forest Ecology and Management 279 : 66 - 76 .
Griggs JA , Rock JH , Webster CR , Jenkins MA . 2006 . Vegetative legacy of a protected deer herd in Cades Cove, Great Smoky Mountains National Park . Natural Areas Journal 26 : 126 - 136 .
Hobbs NT , 1996 . Modification of ecosystems by ungulates . Journal of Wildlife Management 6 : 695 - 713 .
Horsley SB , Stout SL , De Calesta DS . 2003 . White-tailed deer impact on the vegetation dynamics of a northern hardwood forest . Ecological Applications 13 : 98 - 118 .
Hurley PM , Webster CR , Flaspohler DJ , Parker GR . 2012 . Untangling the landscape of deer overabundance: reserve size versus landscape context in the agricultural Midwest . Biological Conservation 146 : 62 - 71 .
Hutchinson FT , Vankat JL . 1997 . Invasibility and effects of Amur honeysuckle in Southwestern Ohio Forests . Conservation Biology 11 : 1117 - 1124 .
Jacobs DF . 2003 . Nursery production of hardwood seedlings . Purdue University Cooperative Extension Service, FNR-212. West Lafayette, IN, 8p .
Jacobs DF , Dalgleish HJ , Nelson CD . 2013 . Tansley review A conceptual framework for restoration of threatened plants: the effective model of American chestnut (Castanea dentata) reintroduction . New Phytologist 197 : 378 - 393 .
Jacobs DF , Oliet JA , Aronson J , et al. 2015 . Restoring forests: what constitutes success in the twenty-first century? New Forests 46 : 601 - 614 .
Jenkins LH , Jenkins MA , Webster CR , Zollnerd PA , Shields JM . 2014 . Herbaceous layer response to 17 years of controlled deer hunting in forested natural areas . Biological Conservation 175 : 119 - 128 .
Joesting HM , McCarthy BC , Brown KJ . 2009 . Determining the shade tolerance of American chestnut using morphological and physiological leaf parameters . Forest Ecology and Management 257 : 280 - 286 .
LaGory MK , LaGory KE , Taylor DH . 1985 . Winter browse availability and use by white-tailed deer in southeastern Indiana . Journal of Wildlife Management 49 : 120 - 124 .
Loftis DL. 1990 . A shelterwood method for regenerating red oak in the southern Appalachians . Forest Science 36 : 917 - 929 .
Loomis JD , Matter SF , Cameron GN . 2015 . Effects of invasive Amur honeysuckle (Lonicera maackii) and white-tailed deer (Odocoileus virginianus) on survival of sugar maple seedlings in a Southwestern Ohio forest . American Midland Naturalist 174 : 65 - 73 .
Lovett GM , Weiss M , Liebhold AM , et al. 2016 . Nonnative forest insects and pathogens in the United States: impacts and policy options . Ecological Applications 26 : 1437 - 1455 .
Luken JO , 1997 . Conservation in the context of non-indigenous species . In: Schwartz MW, ed. Conservation in highly fragmented landscapes. New York: Chapman and Hall, 117 - 134 .
Luken JO , Thieret JW . 1994 . Amur honeysuckle, its fall from grace . BioScience 46 : 18 - 24 .
Mallya G , Zhao L , Song XC , Niyogi D , Govindaraju RS . 2013 . 2012 Midwest drought in the United States . Journal of Hydrologic Engineering 18 : 737 - 745 .
McCune B , Mefford MJ . 2011 . PC-ORD . Multivariate analysis of ecological data. Version 6 (computer program) . MjM Software , Gleneden Beach, OR , USA.
McEwan RW , Arthur-Paratley LG , Rieske LK , Arthur MA . 2010 . A multiassay comparison of seed germination inhibition by Lonicera maackii and co-occurring native shrubs . Flora 205 : 475 - 483 .
McGeehan SL , Naylor DV . 1988 . Automated instrumental analysis of carbon and nitrogen in plant and soil samples . Communications in Soil Science and Plant Analysis 19 : 493 - 505 .
Merriam RW , Feil E. 2002 . The potential impact of an introduced shrub on native plant diversity and forest regeneration . Biological Invasions 4 : 369 - 373 .
Minor ES , Tessel SM , Engelhardt KAM , Lookingbill TR , 2009 . The role of landscape connectivity in assembling exotic plant communities: network analysis . Ecology 9 . 1802 - 1809 .
Murray BD , Webster CR , Bump JK , 2013 . Broadening the ecological context of ungulate-ecosystem interactions: the importance of space, seasonality, and nitrogen . Ecology 9 . 1317 - 1326 .
Natural Resources Conservation Service . 2016 . United States Department of Agriculture. Web Soil Survey . http://websoilsur vey. nrcs.usda.gov/ (16 November 2015 ).
Nelson DW , Sommers LE , 1996 . Total carbon, organic carbon and organic matter . In: Bartels JM , et al., ed. Methods of soil analysis: Part 3. Chemical methods. 3rd edn. Madison, WI: ASA and SSSA Book Series 5 , 961 - 1010 .
Oswalt CM , Fei S , Guo Q , Iannone BV , Oswalt S , Pijanowski B , Potter KM . 2015 . A subcontinental view of forest plant invasions using national inventory data . Neobiota 24 : 49 - 54 .
Paillet FL , 2002 . Chestnut: history and ecology of a transformed species . Journal of Biogeography 2 . 1517 - 1530 .
Paquette A , Bouchard A , Cogliastro A. 2006 . Survival and growth of underplanted trees: a meta-analysis across four biomes . Ecological Applications 16 : 1575 - 1589 .
Pfeiffer SS , Gorchov DL . 2015 . Effects of the invasive shrub Lonicera maackii on soil water content in eastern deciduous forest . American Midland Naturalist 173 : 38 - 46 .
Pike N. 2011 . Using false discovery rates for multiple comparisons in ecology and evolution . Methods in Ecology and Evolution 2 : 278 - 282 .
Pitt DG , Comeau PG , Parker WC , et al. 2010 . Early vegetation control for the regeneration of a single-cohort, intimate mixture of white spruce and trembling aspen on upland boreal sites . Canadian Journal of Forest Research 40 : 549 - 564 .
Pitt DG , Morneault A , Parker WC , Stinson A , Lanteigne L , 2009 . The effects of herbaceous and woody competition on planted white pine in a clearcut site . Forest Ecology and Management 2 . 1281 - 1291 .
Pogge FL . 1967 . Elm as deer browse . Journal of Wildlife Management 31 : 354 - 356 .
Poulette MM , Arthur MA . 2012 . The impact of the invasive shrub Lonicera maackii on the decomposition dynamics of a native plant community . Ecological Applications 22 : 412 - 424 .
R Core Team . 2013 . R: A language and environment for statistical computing . R Foundation for Statistical Computing , Vienna, Austria. http://www.R-project. org (16 November 2015 ).
Reyer CPO , Brouwers N , Rammig A , et al. 2015 . Forest resilience, tipping points and global processes . Journal of Ecology 103 : 1 - 4 .
Ritchie ME , Tilman D , Knops JMH , 1998 . Herbivore effects on plant and nitrogen dynamics in oak savanna . Ecology 7 . 165 - 177 .
Rooney TP , Waller DM . 2003 . Direct and indirect effects of whitetailed deer in forest ecosystems . Forest Ecology and Management 181 : 165 - 176 .
Rossell CR , Gorsira B , Patch S. 2005 . Effects of white-tailed deer on vegetation structure and woody seedling composition in three forest types on the Piedmont Plateau . Forest Ecology and Management 210 : 415 - 424 .
Schuster MJ , Dukes JS . 2014 . Non-additive effects of invasive tree litter shift seasonal N release: a potential invasion feedback . Oikos 123 : 1101 - 1111 .
Shelton AL , Henning JA , Schultz P , Clay K. 2014 . Effects of abundant white-tailed deer on vegetation, animals, mycorrhizal fungi, and soils . Forest Ecology and Management 320 : 39 - 49 .
Shields JM , Jenkins MA , Saunders MR , Zhang H , Jenkins LH , Parks AM . 2014 . Age distribution and spatial patterning of an invasive shrub in secondary hardwood forests . Forest Science 60 : 830 - 840 .
Shields JM , Jenkins MA , Saunders MR , Gibson KD , Zollner PA , Dunning JB . 2015a . Influence of intensity and duration of invasion by Amur honeysuckle (Lonicera maackii) on mixed hardwood forests of Indiana . Invasive Plant Science and Management 8 : 44 - 56 .
Shields JM , Saunders M , Gibson K , Zollner P , Dunning J , Jenkins M. 2015b . Short-term response of native flora to the removal of non-native shrubs in mixed-hardwood forests of Indiana, USA . Forests 6: 1878 - 1896 .
Sotala DJ , Kirkpatrick CM . 1972 . Foods of white-tailed deer, Odocoileus virginianus , in Martin County, Indiana. American Midland Naturalist 89 : 281 - 286 .
Therneau T. 2015 . A Package for Survival Analysis in S. version 2 .38, http://CRAN.R-project.org/package¼survival.
Tilghman N. 1989 . Impacts of white-tailed deer on forest regeneration in northwestern Pennsylvania . The Journal of Wildlife Management 53 : 524 - 532 .
U.S. Climate Data . 2015 . http://www.usclimatedata. com/ (9 December 2015 ).
USDA , NRCS. 2015 . The PLANTS Database . National Plant Data Team, Greensboro , NC 27401 -4901 U.S.A. http://plants.usda. gov (16 November 2015 ).
Vavra M , Parks CG , Wisdom MJ . 2007 . Biodiversity, exotic plant species, and herbivory: the good, the bad, and the ungulate . Forest Ecology and Management 246 : 66 - 72 .
Verhoeven KJF , Simonsen KL , McIntyre LM . 2005 . Implementing false discovery rate control: increasing your power . Oikos 108 : 643 - 647 .
Waller D. 2014 . Effects of deer on forest herb layers , In: Gilliam FS, ed. The herbaceous layer in forests of eastern North America . New York: Oxford University Press, 369 - 399 .
Waller DM , Alverson WS . 1997 . The white-tailed deer: a keystone herbivore . Wildlife Society Bulletin 25 : 217 - 226 .
Waring RH , Cleary BD . 1967 . Plant moisture stress: evaluation by pressure bomb . Science 155 : 1248 - 1254 .
Webster CR , Jenkins MA , Jose S. 2006 . Woody invaders and the challenges they pose to forest ecosystems in the eastern United States . Journal of Forestry 104 : 366 - 374 .