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K.B. Welshofer and D.B. Vandermast
22001166 SOUTHEASTERN NATURALIST 1V5o(4l.) :1656,9 N–6o8. 04
Beech Bark Disease Reduces Sus scrofa (Boar) Rooting
Intensity in Great Smoky Mountains National Park
Kileigh B. Welshofer1 and David B. Vandermast2,*
Abstract - This study examines the effect of beech bark disease (BBD) on Sus scrofa (European
Wild Boar) rooting in high-elevation Beech gaps of Great Smoky Mountains National
Park. In 2011, we sampled vegetative cover by stratum (canopy, shrub, herb) and European
Wild Boar rooting extent in pre-existing fenced boar-exclosure plots and corresponding unfenced
plots. We also used data from previous studies to compare frequencies of individual
herbaceous species collected pre-BBD to those collected post-BBD. Our results indicate
that mortality of Fagus grandifolia (American Beech) trees due to BBD and the consequent
growth of a dense shrub-layer significantly reduced boar rooting in gaps within the Beech
stands. We found that herbs were affected by both European Wild Boar and the dense
shrub-cover following American Beech mortality; however, some plant species remained
abundant, possibly because they were protected from detection within the shrubs.
Introduction
Exotic organisms are species that have been introduced to an environment in
which they do not naturally occur. Upon introduction to a new ecosystem, exotic
species can become established and disrupt the ecological niches of the existing native
organisms in the region (Atkinson 1996, Donlan and Wilcox 2008). Although
the subject of invasive species has been widely studied throughout the last century,
little is known about the interactions among 2 or more invasive species within the
ecosystem they have invaded.
Since its migration into Great Smoky Mountains National Park (GRSM) from
a nearby hunting preserve during the 1940s, Sus scrofa L. (European Wild Boar,
hereafter Boar) has been causing reductions in species richness and diversity by
rooting through the forest understory (Bratton 1975, Jones 1959). Fagus grandifolia
(American Beech, hereafter Beech) forests in high-elevation (>1524 m)
forest stands are the preferred summer habitat for the omnivorous Boars, supplying
them with an abundance of diverse herbaceous plants and other organisms for
consumption. Foraging by ungulates, such as that conducted by Boars, is known
to drastically change forest ecosystems (Russell et al. 2001). Rooting is known to
cause damage to tree roots, and destroy seedlings and wildflowers, which reduces
understory cover and diversity in GRSM (Bratton 1974) both through direct consumption
and by uprooting of non-target plants in search of food.
Beech bark disease (BBD) was first documented at GRSM in 1993, where this
invasive insect–fungal-pathogen complex was identified as killing mature Beech
1Department of Environmental Studies, Elon University, Elon, NC 27244. 2Department of
Biology, Elon University, Elon, NC 27244. Corresponding author - dvandermast@elon.edu.
Manuscript Editor: John Riggins
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2016 Vol. 15, No.4
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trees near Clingman’s Dome (Houston 1994). Following its discovery in 1993,
BBD spread throughout eastern GRSM Beech forests, but had not, as of the time of
data collection for this study, extended to the far-western Beech gaps. The combination
of the Cryptococcus fagisuga Lindinger (Beech Scale Insect) and 1 of 2 fungal
species, commonly Nectria coccinea var. faginata Desm. and less-commonly
Nectria galligena (Bres.) Rossman & Samuels, has led to the death of as many as
90% of American Beech trees in some high-elevation forests. Mature Beech (in
excess of 8 cm DBH) experience the greatest mortality—smaller trees are often
not infested by the scale insect (Vandermast 2005). The disease is initiated with the
establishment of the insect, and alteration of the Beech bark. The Nectria fungus is
then able to infect the lateral meristematic tissue, eventually girdling the tree and
dissociating the bark from the sapwood, a characteristic unique to BBD (Ehrlich
1934, Mahoney et al. 1999) that allows for accurate forensic determination of the
cause of tree death.
Beech bark disease has been shown to have complex effects on the vegetative
community. It causes significant reduction in above-ground biomass and alters the
dominance of Beech in the forest canopy (Forrester et al. 2003). In GRSM, Beech
forests suffering a reduction in canopy coverage because of BBD are rapidly colonized
by dense thickets—sometimes in excess of 30 stems/m2—of Beech sprouts
and Rubus canadensis L. (Blackberry) (Vandermast 2005).
Beech trees may also be affected by Boar rooting. Beech sprouts have been
found to be significantly taller and more abundant when exposed to loosened soils
and other rooting conditions (Howe et al. 1981). This change in composition and
density of the understory may alter the availability of food resources and accessibility
of Beech forests to Boars. Further, the lack of mature Beech canopy due to BBD
has changed the vegetation of the forest floor (Morin and Liebhold 2015). In the
Beech gaps of GRSM, these changes have led to a greater density of sapling-sized
Beech trees and dense thickets of Blackberry canes (Vandermast 2005).
In this study, we examined the (1) extent to which BBD-induced changes in
forest structure affected Boar rooting, and (2) extent to which these changes impacted
the frequency of specific plant species in the high-elevation Beech forests
of GRSM. We hypothesized that death of the Beech canopy due to BBD reduced
the extent of Boar rooting in high-elevation Beech forests in GRSM. Furthermore,
we hypothesized that herbaceous species capable of existing in the dense thickets
of Beech sprouts and Blackberry undergo a reprieve from Boar rooting and occur
at higher frequencies than they would in forests with Boar rooting.
Field-site Description
High-elevation Beech gaps are a unique forest type dominated by Beech trees
(relative abundance is >50%). They are typically located on southward-facing
slopes in the gaps between mountain peaks (Whittaker 1956). Beech trees within
the gaps are nearly genetically identical due to their clonal reproduction through
root sprouts of canopy trees (Morris et al. 2004). Beech gaps are deciduous islands,
often entirely surrounded by spruce–fir forests throughout the high elevations of the
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2016 Vol. 15, No. 4
park (Russell 1953). Two dominant types of understory occur within the Beechgap
ecosystem: an open and Carex spp.-dominated habitat with some shrubs, and
one with a diverse, forb-dominated herbaceous layer that is enhanced by the dense
shade provided by the canopy (Whittaker 1956). Boars appear to avoid rooting in
Beech gaps where sedges are the dominant understory plants; therefore, in this
study we only utilized plots in Beech forests where the understory was forb-dominated
(Vandermast 2005).
We sampled 20 pre-existing plots, including 10 Boar “exclosures” and 10 corresponding
“control” (non-exclosure) plots (see Supplemental File 1, available online
at http://www.eaglehill.us/SENAonline/suppl-files/s15-4-S2277-Vandermast-s1,
and, for BioOne subscribers, at http://dx.doi.org/10.1656/S2277.s1). Exclosures
consist of a chain-link fence up to 1.8 m (6 ft) high that protected part of the Beech
gap from Boar rooting. The Boar exclosures and control plots were established in
the 1980s by GRSM personnel specifically for the purpose of studying the effects
of Boar rooting on Beech-gap flora. The exclosures vary in size from just over 100
m2 to >1 ha. In all cases, the areas sampled in the exclosures and the control plots
were equal.
Methods
During the summer of 2011, we followed the Carolina Vegetation Survey (CVS;
Peet et al. 1998) protocol to sample tree, shrub, and herb cover in 10 exclosure and
10 corresponding unfenced control plots. Trees tend to grow slowly and are often
stunted in high-elevation Beech gaps. The tree canopy typically consists of Beech
with a few co-occurring species and is usually 18–22 m tall. Shrub cover ranges
from 2–2.5-m high and consists of Blackberry and tree saplings (mostly Beech).
Herb cover is less than 1 m tall.
The standard unit of observation in the CVS protocol is the 100-m2 module.
We estimated the area affected by Boar rooting within each module. For purposes
of consistency, we estimated Boar-rooting area in the same way as the vegetation
cover. Boar rooting is identifiable from other forms of animal rooting in Beech
forests because Boars overturn much larger patches of forest floor (often in excess
of 100 m2), compared to Ursus americanus (Pallas) (American Black Bear) and
Odocoileus virginiana Zimmermann (White-tailed Deer), which only scrape soil in
distinct locations (usually less than 10 m2). It is not an exaggeration to say that Boar rooting
resembles rototilling of the forest soil.
We analyzed the relationship between BBD-caused Beech mortality and Blackberry
cover in both exclosure and control plots because BBD killed Beech trees in
both areas. We examined the relationship between Blackberry cover and the Boar
rooting in control plots only because these were the only areas accessible to Boars.
In both cases, we used correlation analysis to examine these relationships. Furthermore,
we separated Beech forests into those with high levels of Beech mortality
(n = 12) and those with low levels of Beech-mortality (n = 8). High-mortality plots
contained many dead Beech trees with the characteristic mortality pattern caused
by BBD. Low-mortality sites were those where BBD had not yet begun to kill
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Beech trees, and mortality in these plots appeared to be representative of normal
background tree-mortality rates. We compared Blackberry cover and Boar rooting
between high- and low-mortality plots using a two-sample t-test (a = 0.05) in SigmaPlot
v.9.0 (Systat Software, Inc., San Jose, CA).
We did not collect data on individual herbaceous species. Thus, in order to examine
changes in individual species over time, we used data collected by Russell in
1953 (prior to the introduction of both BBD and Boars to the Beech gaps he studied)
to compare with data collected by Kay and Vandermast 2009, which was the most
recently collected usable data. Also, because Russell’s paper only reported frequency
data for herbs, we converted the 2008 species cover data to frequency values
for comparison purposes. The 2008 data were collected using the CVS protocol in
the same exclosure and control plots used in our 2011 study. Thus, we were able
to compare frequencies of plant species in Beech gaps from pre-exposure (Russell
1953 data) to those exposed only to BBD (2008 exclosure data), and those exposed
to both rooting and BBD (2008 unfenced-control data).
Bratton’s (1974) paper predicted that boar rooting would harm certain herbaceous
species in GRSM Beech gaps. To use Bratton’s species list to compare
Russell data with our 2008 data, we categorized susceptible species as follows:
Aster spp. (asters), Carex spp. (sedges), Lilium superbum L. (Turks-cap Lily),
Monarda didyma L. (Bee Balm), and Poa alsodes A. Gray (Grove Bluegrass), Rudbeckia
laciniata L. (Cutleaf Coneflower), Trillium erectum L. (Wake Robin), and
Viola spp. (violets). In addition, there were plant species documented by Russell
that were not predicted by Bratton to be threatened by Boar rooting. Those species
include Angelica triquinata Michx. (Filmy Angelica), Cuscuta sp. (dodder),
Houstonia serpyllifolia Michx. (Thymeleaf Bluet), Oxalis montana Raf. (Mountain
Woodsorrel), and Blackberry.
Results
Across the Beech gaps in this study, we found a negative correlation (r = -0.522,
r2 = 0.272) between canopy cover and shrub cover, confirming previous observations
that shrub cover increases with the death of the Beech canopy (Fig. 1). There
is much variation in our data, but it appears that when canopy cover is less than 60%,
Blackberry cover increases dramatically in most plots. Beech forests with >60%
canopy cover had low Blackberry cover.
Furthermore, we found that there was a strong, negative correlation between the
area affected by Boar rooting and shrub-cover (r = -0.925, and r2 = 0.856; Fig. 2).
In forests where Blackberry cover was >70%, the area affected by Boar rooting
declined to almost nothing. We noted that game trails were evident in the dense
Blackberry thickets, and Boars likely used these trails.
The area of Beech forests affected by Boar rooting was significantly higher at
sites with low levels of Beech mortality (32.7 ± 5.23%) than in those with high
levels of Beech mortality (1.6 ± 0.5%) (2-sample t-test: P < 0.01, df = 9; Fig. 3).
Shrub-cover was high (83.3 ± 11.5%) in plots with high mortality (tree cover = 16.3
± 14.2%) but low (16.3 ± 12.9%) in plots experiencing low mortality (tree cover =
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2016 Vol. 15, No. 4
64.7 ± 10.6%). We found no statistical evidence for a difference in average percentage
of herb-cover in high-mortality vs. low-mortality plots (2-sample t-test: P =
0.69, df = 19). However, it is likely that different species of herbs were present in
plots with low vs. high levels of Beech mortality.
Figure 2. Correlation between shrub cover and Boar rooting in unfenced control plots in
high-elevation Beech gaps in Great Smoky Mountains National Park.
Figure 1. Correlation between shrub cover and American Beech canopy cover in highelevation
Beech gaps in Great Smoky Mountains National Park.
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All of the species Bratton (1974) predicted to be susceptible to Boar rooting
occurred at lower frequencies in the 2008 data (post-BBD) than when observed
pre-BBD by Russell. Of particular interest, Turk’s-cap lily, which occurred at a frequency
of nearly 40% in the Russell data, was almost non-existent in the 2008 data
(Fig. 4). Also, for all species except asters and sedges, the frequencies were higher
in the unfenced control plots where these plants were subject to the effects of both
Boar rooting and BBD than in the plots where Boars were excluded.
Of the additional herbaceous species, Blackberry and dodder occurred more
frequently in 2008 than in the pre-BBD data (Fig. 5). Mountain Woodsorrel, which
Figure 4. Frequencies of herbaceous species identified by Bratton (1974) as being susceptible
to Boar rooting. The pre-BBD frequencies are from Russell (1953), the Rooting/BBD
data are from 2008 unfenced controls where plants were subject to both rooting and BBD,
and BBD only data are from Boar exclosures where plants were subject only to BBD.
Figure 3. Average percent
of plot area affected by
Boar rooting in Beech forests
with high levels of
Beech mortality due to
BBD (32.7%) vs. low levels
of Beech mortality (1.6%)
(P < 0.01). Plots with high
mortality had numerous
trees exhibiting the characteristic
mortality pattern
caused by BBD. Plots with
low mortality were in areas
that BBD had not yet
reached. The low mortality
represents a background
mortality rate.
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2016 Vol. 15, No. 4
occurred at a frequency of almost 40% in the 1953 data, was not observed in 2008
and Thymeleaf Bluet was observed far more frequently in unfenced plots than in
exclosures.
Our analysis of tree species identified both by Russell (1953) and in 2008 indicates
that all tree species occurred at reduced frequencies in the later data set
(Table 1). This finding could be due to a combination of BBD and Boar rooting,
but high-elevation forests in GRSM are subject to many modern stressors including
excess nitrogen input and ozone damage. Four species commonly found in Beech
forests in 2008 were not listed by Russell in his study: Acer saccharum (Sugar
Table 1. Frequencies (% of modules in which a tree occurred) of tree species in 1953 and 2008. In
2008, trees in control plots were subject to both BBD and Boar rooting and trees in exclosures were
subject to BBD only.
1953 Frequency 2008 Frequency
Tree Species Russell Total Control Exclosure
Acer pensylvanicum L. (Striped Maple) 29 8.3 11.8 3.8
Abies fraseri (Pursh) Poir. (Frasier Fir) 36 13.3 11.8 15.4
Acer rubrum L. (Red Maple) 21 3.3 0.0 7.7
Amelanchier laevis Wiegand (Smooth Shadbush) 43 6.7 0.0 15.4
Betula alleghaniensis Britton (Yellow Birch) 50 38.3 38.2 38.5
Fagus grandifolia Ehrh. (American Beech) 100 70.0 79.4 57.7
Picea rubens Sarg. (Red Spruce) 86 23.3 35.3 7.7
Prunus serotina Ehrh. (Black Cherry) 29 13.3 8.8 19.2
Acer saccharum Marsh. (Sugar Maple) 38.3 38.2 38.5
Acer spicatum Lam. (Striped Maple) 23.3 5.9 46.2
Aesculus flava Sol. (Yellow Buckeye) 26.7 29.4 23.1
Quercus rubra L. (Red Oak) 16.7 8.8 26.9
Figure 5. Frequencies of herbaceous species that Bratton (1974) did not predict as being
susceptible to Boar rooting. These are species that displayed a difference in the frequency
observed between pre-BBD and Boar introduction in 1953 and post-BBD and Boar introduction
in 2008.
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Maple), A. spicatum (Mountain Maple), Aesculus flava (Buckeye), and Quercus
rubra (Red Oak). Of these 4 species, 2 occurred at higher frequencies in exclosures
than in control plots; Mountain Maple occurred in 46.2% of exclosures and 5.9%
of controls, and Red Oak occurred in 26.9% of exclosures and 8.8% of controls.
This observation suggests these species are susceptible to Boar rooting or other
disturbances prevented by the exclosure fencing.
Discussion
In this study, we examined how 1 invasive species, BBD, could alter the use of
high-elevation Beech forests in GRSM by another invasive species, the European
Wild Boar. Our results indicate that the increase in Blackberry cover following
canopy Beech death from BBD reduced the amount of Boar rooting in these forests.
Boar rooting was most likely reduced because the dense blackberry growth inhibited
access and reduced resources for the Boars.
Dense Blackberry growth following deforestation or death of canopy trees is
not unique to the high-elevation Beech forests of GRSM. Rapid Blackberry growth
in southern Appalachian clear-cuts has been associated with slow growth of shadeintolerant
species during secondary succession (Wilson and Shure 1993). Blackberry
has long been an important colonizer of high-elevation forest gaps in GRSM (Crandell
1958), but its rate of colonization, density, persistence, and consequent capacity
to inhibit forest reorganization on these sites may be enhanced by atmospheric-N
deposition (Tilman 1987). Atmospheric-N deposition is highest at high elevations
in GRSM (Fowler et al. 1988), and N-mineralization is highest in high-elevation
hardwood forests when rates are compared among different plant communities along
an elevational gradient (Knoepp and Swank 1998). At densities of 30 stems/m2 (Vandermast
2005), Blackberry inhibits the access Boars would normally have to these
forests and likely decreases food availability for them. As a corollary, our data also
showed that Boar rooting was greatly reduced in Beech forests with high mortality
versus those free of BBD with low mortality. While our data show that the dense
shrub layer is likely to exclude Boars from accessing these areas, it is also possible
that the lack of beech nuts once produced by mature beech trees prior to BBD could
also decrease the likelihood of Boars foraging in these areas.
BBD has complex effects on the vegetative communities where it occurs. The
disease causes a significant reduction in above-ground biomass and decreases
the dominance of Beech in the forest canopy (Forrester et al. 2003). Results
from a previous study suggested that, although tree species such as Picea rubens
(Red Spruce) and Sugar Maple become more abundant in diseased Beech forests,
Beech sprouts remain the most abundant regenerating species. In a healthy Beech
gap ecosystem, the shade provided by the canopy suppresses the germination
and growth of Blackberry, leaving room for the regrowth of Beech trees (Vandermast
2005). When BBD kills the mature Beech trees, the canopy no longer
provides shade for the forest understory. The additional sunlight reaching the forest
floor changes the microclimate of the area and leads to changes in vegetative
composition (Gehlhausen et al. 2000), including rapid Blackberry growth.
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Shrubs can consume much of the forest’s space and nutrients; thus, understory
plants normally found in a healthy Beech forest may not be able to acquire essential
resources for survival (i.e., sunlight, soil nutrients). A study in northern
California found that the development of a dense shrub layer affected herbaceous
species abundance of native grasslands. The study showed a decline in many herbaceous
species after the invasion of Baccharis pilularis DC. (Coyote Brush).
However, some shade-tolerant species may benefit from the protection from
predators provided by the shrub layer (Hobbs and Mooney 1986). In our study,
some herbaceous species (trilliums and violets, in particular) in Beech gaps had
higher frequencies in our control plots, where Boars had access. These herbs may
have survived Boar rooting, or become reestablished after it, and can grow in and
among the Blackberry canes where they are protected from rooting.
Bratton’s predictions that certain herbaceous species would be susceptible to
Boar rooting were borne out by the results of our analysis. Our data indicated that,
while all herbaceous species survived in Beech gaps, all of Bratton’s susceptible
groups occurred at lower frequencies in the 2008 data than they did in the 1953
data. Interestingly, within the 2008 data, some of these species occurred at higher
frequencies in areas where they were susceptible to Boar rooting than they did in
the exclosures. We propose that rooting in the control plots may have increased
the frequency of these species compared to the exclosures for several reasons.
First, competition from other plant species because of the lack of rooting within
the exclosures could exclude these species from growing within the plots. Second,
the upturned soils resulting from rooting could provide better habitat for seedling
germination than a forest floor with thick leaf litter. Rooting has been shown to
enhance plant species richness in wetland habitats (Arrington et al. 1999). Seed
dispersal may also increase with Boar rooting. A study in Germany found that
Boar rooting increased the dispersal distance of species across forested and open
ecosystems (Heinken et al. 2005). However, the difference in effects of BBD and
Boar rooting on the herbaceous community of Beech gaps is difficult to distinguish
because of the ubiquitous nature of the disease. Additionally, the exclusion of all
foraging species within the exclosure plots may also affect the presence of herbaceous
species.
Some species recorded by Russell in 1953 that were not considered by Bratton
as susceptible to rooting declined in frequency while others increased. Two species
found more commonly in 2009 than in 1953 were Blackberry and dodder. The
increase in Blackberry frequency is due to the mortality of canopy Beech trees.
Dodder regularly parasitizes Blackberry in the southern Appalachians (Radford
1968) and would be expected to increase in frequency proportional to the increase
in Blackberry frequency (Musselman 1986).
It is possible that some of the differences in frequencies noted in this study compared
to present studies could be due to the differences in sampling seasons (Bratton
and Russell in early-mid summer and 2008 data collected in early August). Some
herbs that emerge in the spring may have completed the above-ground part of their
lifecycle by early August. If this is the case, the 2008 data may have underestimated
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frequency. However, given that all species except Mountain Woodsorrel were observable
in early August, it is unlikely that this difference is meaningful.
Our results suggest that the effects BBD on the structure of Beech gaps could
limit Boar rooting in Beech gaps and possibly provide a temporary hiatus from rooting
for species capable of surviving in the Beech sprout and Blackberry thickets
that develop following the death of the canopy Beech trees.
Restoration of the Beech gaps to their pre-BBD structure and composition seems
unlikely. The reduced rooting of Boars because of the dense shrub layer is not a
permanent solution to protecting existing plant species in Beech gaps. As noted,
many species continue to decline with the presence of both the Boar and BBD in
Beech forests. While it is certainly possible that excess nitrogen-deposition, warming
temperatures, and ozone alter plant populations in these forests, we found that
Boar rooting and the dense growth of Blackberry change the frequencies of some
species. Beech saplings and other trees will eventually grow tall enough to shade
the Blackberry thickets, which will become less dense and even disappear from
the forest. This transition will return the forest to an approximation of its pre-BBD
structure, but it also will provide enhanced conditions for Boar rooting. The control
of either invasive species (BBD or Boar) is extremely difficult. Despite control
methods, the Boar population continues to increase steadily (Peine and Farmer
1990), and controlling BBD is difficult because of its wide dispersal throughout the
park and surrounding areas as well as the complexities of the lifecycles of the insect
and fungal species.
Acknowledgments
We are grateful for the Southern Appalachian Botanical Society’s Earl Core Award and
the Elon College Fellows program for financial support for this project. We thank Alexandra
Kay for use of her data, Monika Hayleck and Cole Vandermast for their help in the field, and
Great Smoky Mountains National Park for permits to work within the park.
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