Microhabitat Selection of the Virginia Northern Flying
Squirrel (Glaucomys sabrinus fuscus Miller) in the Central
Appalachians
Corinne A. Diggins and W. Mark Ford
Northeastern Naturalist, Volume 24, Issue 2 (2017): 173–190
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Northeastern Naturalist Vol. 24, No. 2
C.A. Diggins and W.M. Ford
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2017 NORTHEASTERN NATURALIST 24(2):173–190
Microhabitat Selection of the Virginia Northern Flying
Squirrel (Glaucomys sabrinus fuscus Miller) in the Central
Appalachians
Corinne A. Diggins1,* and W. Mark Ford2
Abstract - Glaucomys sabrinus fuscus (Virginia Northern Flying Squirrel; VNFS) is a rare
Sciurid that occurrs in the Allegheny Mountains of eastern West Virginia and northwest
Virginia. Previous work on this subspecies has confirmed close associations with Picea
rubens (Red Spruce) at the landscape and stand levels in the region. However, ongoing Red
Spruce restoration actions using canopy-gap creation to release single or small groups of
trees requires a better understanding of within-stand habitat selection of VNFS to assess
potential short- and medium-term impacts. To address these questions, we conducted a
microhabitat study using radio-collared squirrels in montane conifer and mixed conifer–
hardwood stands. We used points obtained from telemetry surveys and randomly generated
points within each squirrel’s home range to compare microhabitat variables for 13 individuals.
We found that VNFS preferentially selected plots with conifer-dominant overstories and
deep organic-soil horizons. VNFS avoided plots with dense Red Spruce regeneration in the
understory in stands with hardwood-dominated overstories—the types of areas targeted for
Red Spruce restoration. We also opportunistically searched for hypogeal fungi at telemetry
points and found 3 species of Elaphomyces during our surveys. Our results indicate that
microhabitat selection is associated with Red Spruce-dominant forests. Efforts to restore
Red Spruce where hardwoods dominate in the central Appalachians may improve the connectivity
and extent of habitat of VNFS.
Introduction
Glaucomys sabrinus fuscus Miller (Virginia Northern Flying Squirrel; VNFS)
is a rare subspecies of G. sabrinus (Shaw) (Northern Flying Squirrel) found in
montane conifer and conifer–northern hardwood forests in the central Appalachian
Mountains of eastern West Virginia and western Virginia (Reynolds et al. 1999,
Stihler et al. 1995). The preferred habitat of the VNFS is Picea rubens Sarg. (Red
Spruce)-dominated forests (Ford et al. 2007, Menzel et al. 2006, Stihler et al. 1995).
This forest type has been reduced from an estimated >200,000 ha in the late 1800s
to less than 20,000 ha at present (Byers et al. 2013, Korstian, 1937, Newins 1931,
Schuler et al. 2002) due to industrial clear-cut logging and subsequent fires during
the early to mid-20th century (Clarkson 1964). Since that time, spruce forests have
been further degraded by acid precipitation (Eagar and Adams 1992) and exotic
pests (i.e., Adelges picea Ratzeburg [Balsam Woolly Adelgid]) and are projected
to be highly vulnerable to future anthropogenic climate change (Beane and Rentch
1Department of Fisheries and Wildlife Conservation, Virginia Polytechnic Institute and State
University, Blacksburg, VA, 24061. 2US Geological Survey, Virginia Cooperative Fish and
Wildlife Research Unit, Blacksburg, VA, 24061. *Corresponding author - cordie1@vt.edu.
Manuscript Editor: Thomas W. French
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2015). Noss et al. (1995) listed Red Spruce-dominated forests of the region as one
of the most critically endangered forested ecosystems in the US because of its reduced
extent and recent degradation.
Multiple studies indicated a positive relationship between the VNFS and Red
Spruce forest at the landscape (Ford et al. 2010, Menzel et al. 2005, Odom et al.
2001) and stand level in the region (Ford et al. 2007; Menzel et al. 2004, 2006).
In the Appalachians, past research indicated that denning habitat often has been
associated with the northern hardwood–conifer ecotone (Hackett and Pagels 2003,
Weigl et al. 1999). However, radio-collared VNFS in the central Appalachians
and endangered G. s. coloratus Howell (Carolina Northern Flying Squirrel) in the
southern Appalachians use Red Spruce as foraging habitat more than expected
based on their availability (Diggins 2016; Ford et al. 2007, 2014; Menzel et al.
2006). This preference may be due to the greater abundance of important food items
(i.e., hypogeal fungi; Mitchell 2001) for these subspecies in montane conifer versus
northern hardwood forests (Loeb et al. 2000). Many nest-box locations for both
subspecies are biasedly placed in the montane conifer–northern hardwood ecotone,
where denning was thought to exclusively occur (Ford et al. 2010), although recent
research suggests these subspecies readily den in Red Spruce-dominated stands
(Diggins 2016, Diggins et al. 2015, Ford et al. 2010, 2014). Habitat use by this
subspecies has been studied on larger scales, but within-stand habitat associations
are not well-defined.
VNFS was listed as endangered under the Endangered Species Act in 1985
(USFWS 1985), and subsequently delisted in 2013 (USFWS 2013). The delisting
occurred because the majority (63%) of VNFS habitat is protected on public land,
and nest-box occupancy rates were indicative of long-term persistence, as determined
from long-term nest-box monitoring data (Ford et al. 2010, Menzel et al.
2005). Paradoxically, the delisting of this subspecies has allowed more-flexible
habitat management strategies to improve habitat quality and connectivity than
when it was listed, including ecological restoration of Red Spruce forests using
canopy-gap creation (Rentch et al. 2007, 2010, 2016; Schuler et al. 2002).
Presently, the VNFS is a focal rationale for Red Spruce restoration in the central
Appalachians because these activities are designed to increase the extent and connectivity
of the squirrel’s habitat. However, biologists and land managers are still
debating what constitutes the preferred habitat of this subspec ies. This discussion
centers on determining which habitat type is more important to the VNFS: montane
conifer forests (i.e., Red Spruce, and Tsuga canadensis [L.] Carr. [Eastern
Hemlock]) or high-elevation northern hardwood forests dominated by Betula alleghaniensis
Britton (Yellow Birch), Fagus grandifolia Ehrh. (American Beech)
and other species (i.e., forest types adjacent to Red Spruce stands that may be designated
for restoration treatments).
Red Spruce, a shade-tolerant species, has been increasing in extent as understory
regeneration in areas where northern hardwoods became dominant
following logging and burning in the past 100 years (Mayfield and Hicks 2010,
Rollins et al. 2010). This process may reflect signs of natural recovery of Red
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Spruce forests (Nowacki et al. 2010), although natural recovery is gradual due to
the slow establishment characteristics of Red Spruce (Rentch et al. 2010, Smith
and Nicholas 1999, White et al. 1985). Spodic soils with deep organic horizons
are correlated with Red Spruce forests, and evidence of these soil types may still
be present under forests that regenerated as hardwoods after industrial logging
(Nauman et al. 2015). Restoration using single-canopy gap to small-group selection
cuts permit suppressed mid- and understory Red Spruce to be released for
eventual accession to the overstory at a faster rate than natural recovery through
successional trajectories (Rentch et al. 2016). Accelerating the process allows
Red Spruce to regain its status as a foundation species that drives the structure
and processes within the ecosystem (Ellison et al. 2005). Priority sites for Red
Spruce restoration are determined by comparing current Red Spruce cover to its
historic extent (i.e., Byers et al. 2013, Korstian 1937, Nauman et al. 2015), and
efforts are underway to identify important habitat patches and corridors for other
Red Spruce-associated wildlife (Rentch et al. 2007). Currently, little research, beyond
anecdotal observations, has examined microhabitat selection by the VNFS,
thereby limiting effective prioritization of future forest-restoration actions for
this subspecies (Ford et al. 2004, Odom et al. 2001).
Our objective was to determine variables that influence within-stand microhabitat
selection by the VNFS in the central Appalachians. We used squirrel locations
obtained from telemetry data of radio-collared individuals, and compared microhabitat
characteristics for selected sites with available sites within a squirrel’s home
range. We hypothesized that VNFS would preferentially select microhabitats associated
with montane conifer forests (i.e., deep organic-soil horizons, and conifer
dominance in overstory and/or understory).
Field-site Description
We conducted our study in Pocahontas and Randolph counties, WV, in the
Allegheny Mountains and Plateau sub-physiographic region of the central Appalachian
Mountains. The region is characterized by broad plateau-like ridges, steep
slopes, and narrow valleys (Byers et al. 2010, Fenneman 1938). The mountains of
the region are capped with Pennsylvanian siltstones and sandstones characterized
by frigid silt or sandy loam soils that are rocky , highly acidic, and low in produc -
tivity (Allard and Leonard 1952, Flegal 1999, Pyle et al. 1982). Our study sites
included Kumbrabow State Forest (KSF; 38°37'10''N, 80°6'25''W), Snowshoe
Ski Resort (SSR; 38°24'50'' N, 79°59'52''W), and the Greenbrier Ranger District
(GRD; 38°41'15''N, 79°44'11''W) in the Monongahela National Forest (Fig. 1).
The site on SSR was dominated by Red Spruce, whereas sites on GRD were
dominated by Red Spruce, Red Spruce–Eastern Hemlock, and northern hardwood
forests composed of Prunus serotine Ehrh. (Black Cherry), Yellow Birch, and
Acer rubrum L. (Red Maple). Sites on KSF were dominated by planted Picea
abies (L.) H. Karst. (Norway Spruce)–Eastern Hemlock and northern hardwood
forests. All sites were second-growth stands, all had been cutover at least once in
the preceding 100 years, and many had experienced multiple reentries to harvest
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merchantable, high-value timber such as Black Cherry. Elevation at the study sites
ranges from 930 m to 1450 m.
Climatic conditions were cool and moist with frequent fog, high annual precipitation
(120–150 cm distributed throughout the year, with >350 cm of average
annual snowfall in the winter months), and mean annual temperature ranging from
6.7 °C to 9.4 °C with the possibility of freezing temperatures all year (Byers et al.
2010, Rentch et al. 2007, Stephenson 1993).
Methods
We captured VNFS using a combination of nest-box and live-trap surveys. We
coordinated nest-box surveys with the annual spring and fall checks conducted by
the West Virginia Division of Natural Resources and the GRD staff (C. Stihler,
WVDNR, Elkins, WV, unpubl. data). We placed nest boxes (33.0 x 12.7 x 12.7 cm
with a 4.4–5.7 cm opening) in single transects per site ranging from 15 to 30 nest
boxes spaced at 30–50-m intervals ([S. Jones, US Forest Service, Barstow, WV,
pers. comm.; Stihler et al. 1987). We mounted nest boxes 4–5 m from the ground
on the trunks of trees and used a ladder to access them during checks . We supplemented
nest-box checks with live trapping using Tomahawk 201 live traps (14 cm
Figure 1. Virginia Northern Flying Squirrel (Glaucomys sabrinus fuscus Miller) microhabitat-
survey sites during 2013 and 2014 in the central Appalachian Mountains of West
Virginia.
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x 14 cm x 41 cm, Tomahawk Live Trap Co., Hazelhurst, WI) baited with a slice of
apple rolled in a peanut butter–molasses–bacon grease–oatmeal mixture. To reduce
trap stress and potential hypothermic effects of trapping, we placed polyfill batting
in each of the traps and partially covered the traps with plastic and duct tape. We
set traps on the ground and on tree boles to increase captures of flying squirrels
(Loeb et al. 1999). We opened traps at dusk and checked them at dawn. We closed
all traps between sunrise and sunset to reduce capture of diurnal species.
We distinguished Virginia Northern Flying Squirrels from sympatric G. volans
L. (Southern Flying Squirrel) by coloration of ventral fur and hind-foot measurement
(Wells-Gosling and Heaney 1984). We recorded sex, age, reproductive
condition, and mass of all VNFS captures. Individuals were tagged with uniquely
numbered ear tags (No. 1005-1, National Band and Tag Company, Newport, MA).
We radio-collared all adult VNFS captures using 3.4-g and 4.0-g PD-2C radiocollars
(Holohil Systems Ltd., Carp, ON, Canada), which represented ≤5% of their
total body weight. Capture and tagging methods were approved by the Virginia
Tech Institutional Animal Care and Use Committee (permit #11-120-FIW).
We radio-tracked individuals and surveyed flying squirrel telemetry locations
during May—July 2013, October 2013, and May–June 2014. To determine home
ranges, we tracked radio-collared flying squirrels for a minimum of 5 nights or until
the radio-collar signal was lost. We used Wildlife Materials TR4-2000S receivers
(Wildlife Materials, Carbondale, IL) and 3-element folding yagi antennas to determine
the location of flying squirrels. Before each nighttime telemetry session, we
located each flying squirrel’s diurnal den to determine the best location for telemetry
stations that night. We obtained telemetry points using close-range (less than 0.4 km)
biangulation by manning 2 fixed stations to take telemetry points simultaneously
to minimize temporal error, with the assumption that animal movements would not
influence telemetry error rates (Schmutz and White 1990). For each survey night,
telemetry stations were located >50 m apart to minimize bearings taken at less than
90°-angles (White 1985). Close-range biangulation is a common technique used
for arboreal squirrels (Ford et al. 2014, Koprowski et al. 2008, Menzel et al. 2006,
Shanley et al. 2013), because these animals are small-bodied, highly mobile, and
typically inhabit small home-ranges (less than 20 ha). We tracked each flying squirrel for at
least 2 h after civil twilight and typically ended surveys before or at midnight, when
flying squirrel activity drastically decreased (Ford et al. 2007, Menzel et al. 2006).
We obtained bearings on individual flying squirrels every 5–10 min to determine
frequent movements associated with nocturnal activity. All personnel were tested
for telemetry bias by using known locations of transmitters hidden in the field and
actual bearings from telemetry stations to the location of the transmitter (White and
Garrott 1990). We calculated our mean telemetry bearing error to be 3° ± 1° (White
and Garrott 1990).
Microhabitat points and home range
We entered locations of stations and biangulation bearings into the software
program LOCATE II (Pacer Co., Truro, NS, Canada) to obtain locations of
individual squirrels. Using all locations for each VNFS, we estimated home ranges
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using 100% minimum convex polygon (MCP) function in Biotas 2.0 (Ecological
Software Solutions LLC, www.ecostats.com/web/Biotaswww.ecostats.com/web/
Biotaswww.ecostats.com/web/Biotas; Figs. 2, 3). We selected MCP because this
estimator assumes use across the home range is continuous; thus, it does not
explicitly depict high- and low-use areas (Getz and Wilmers 2004, Mitchell and
Powell 2008). Our primary use of MCP was simply to define an area of potential
habitat available to a squirrel in proximity to known flying squirrel locations. As
denoted by other home-range estimators, high-use areas may include higher-quality
habitat and random points may not fall in lower-quality habitat, thereby biasing
microhabitat-comparison data. Home-range shapefiles obtained from Biotas were
imported into ArcMap 10.0 GIS (Environmental Systems Research Institute, Inc.,
Redlands, CA. We used ArcMap to randomly generate 20 points within each home
range of all VNFS with ≥30 points, to serve as random points during microhabitat
surveys. We also randomly selected 20 locations obtained from telemetry surveys
(hereafter, telemetry points) for each individual with the stipulation that randomly
selected telemetry fixes must be ≥30 consecutive minutes apart from one another.
Using telemetry points allowed us to compare points selected by a flying squirrel
with random points within the flying squirrel’s home range (Fig. 3).
Figure 2. 100% maximum convex polygon home-range of male Glaucomys sabrinus fuscus
(Virginia Northern Flying Squirrel) at Greenbrier Ranger District in summer 2014 on the
Monongahela National Forest, WV. The original telemetry-point locations. Picea rubens
(Red Spruce) cover from Byers et al. 2013.
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Microhabitat surveys
We surveyed microhabitat variables at random points and telemetry points for
individual Virginia Northern Flying Squirrels. All subspecies of Northern Flying
Squirrels are preferential mycophagists (Maser et al. 1985, 2008); therefore, we tailored
microhabitat plots to specifically look at factors that might influence hypogeal
fungi. At each point, we chose a plot center and established a 10-m diameter circular
plot. We placed a 1 m x 1-m vegetation sampling frame on the plot center to measure
ground vegetation. We followed the microhabitat-measurement protocol provided
by Castleberry et al. (2002) for Neotoma magister Baird (Allegheny Woodrat) in
the Allegheny Mountains as modified based on previous habitat-association studies
on VNFS and Carolina Northen Flying Squirrel (Ford et al. 2004, 2014, 2015;
Menzel et al. 2006; Payne et al. 1989). At each random point and telemetry point, we
qualitatively assessed dominant and co-codominant tree species within the circular
plot. Hypogeal fungi form an obligatory symbiotic relationship with the roots of
certain tree species, aiding host trees in absorption of nutrients and water from the
soil (Harley and Smith 1983); these relationships are critical to tree and forest health
(Amaranthus 1998). Therefore, we measured the distance to the nearest tree within
Figure 3. 100% maximum convex polygon home-range of male Glaucomys sabrinus fuscus
(Virginia Northern Flying Squirrel) at Greenbrier Ranger District in summer 2014 on the
Monongahela National Forest, WV. Randomly selected telemetry plots and randomly generated
random plots where microhabitat surveys were conducted. Picea rubens (Red Spruce)
cover from Byers et al. (2013).
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10 m from the center of the plot and recorded its species and diameter at breast height
(DBH) to determine if host species for hypogeal fungi were located closer to foraging
points than non-host species. We used a spherical densitometer to measure percent
canopy cover at the plot center. We assessed percent groundcover within the subplot
using the following variables: herbaceous vegetation, bare soil/rock, woody debris/
roots, moss/lichen, and duff (i.e., leaf/needle litter). In each plot, we also measured
and averaged 4 systematically sampled soil plugs to determine the depth of the forest
floor (i.e., organic horizon) within the plot.
The fruiting bodies of hypogeal fungi are subterranean (e.g., truffles) and rely on
small mammals, such as Northern Flying Squirrels, for dispersal throughout the forest
(Fogel 1976, Fogel and Trappe 1978, Johnson 1996, Maser et al. 1978). Home
ranges of Northern Flying Squirrels are larger than those of other small mammals
that consume hypogeoal fungi (e.g., Myodes gapperi Vigors (Southern Red-backed
Vole; Orrock and Pagels 2002), and, therefore, the squirrels may have a greater ecological
role in dispersing fungi across the landscape (Loeb et al. 2000). Although
the VNFS has a generalist diet that includes lichens and tree buds (Mitchell 2001),
in West Virginia, they also consume the fruiting bodies of hypogeal fungi; thus, the
location of host trees for hypogeal fungi may influence microhab itat selection.
For telemetry points, we assessed if there were any signs of small-mammal
digging activity in the subplot to indicate foraging for the fruiting bodies of hypogeal
fungi. We recorded 2 types of small-mammal fungal-foraging types: digs
and scratches. We defined a dig or scratch as fresh if there were no debris (i.e., leaf
fragments, needles) or spider webs covering it (Castellano et al. 1999, 2003). We
opportunistically excavated digs within telemetry points and searched for hypogeal
fungi for ≤5 min within 0.5 m2 area of the dig. We destructively sampled, placed
specimens in wax bags, and later identified all hypogeal fungi to species in the lab.
Data analysis
We employed a Spearman’s rank correlation in the R program (version 3.1; R
Development Core Team 2015) to determine if any of our variables were highly
correlated. No variables were significantly correlated and we retained all variables
for subsequent analysis. We compared differences between variables at telemetry
and random points averaged across all individual squirrels. Our data were not normally
distributed; thus, we analyzed data using a permutated multivariate analysis
of variance (PerMANOVA; Anderson 2001). Assumptions of analysis of variance
are not generally met by most biological data, which tend to be highly skewed
or aggregated. The PerMANOVAs use a permutation procedure to assess significance
without requiring that data be normally distributed (Anderson 2001). We ran
PerMANOVAs based on a Euclidean distance matrix with 9999 permutations per
run using package ‘vegan’ (Dixon 2003, Oksanen et al. 2009). We assessed closest
overstory tree by comparing the distance from the plot center to the tree and
tree type (i.e., conifer versus hardwood species). For dominant overstory trees,
we assessed percent conifer presence (i.e., Red Spruce, Norway Spruce, Eastern
Hemlock) averaged across all sites. For understory conifers, we determined if pole
or seedling Red Spruce or Eastern Hemlock trees were present in the understory,
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including regeneration thickets, and averaged the presence across all sites. We ran a
PerMANOVA to compare soil depth at telemetry points with hypogeal fungi versus
telemetry points without hypogeal fungi.
Results
We captured 28 VNFS (21 adults, 7 juveniles) during 746 nest-box checks and
~1300 trap nights. We fitted 19 adult flying squirrels with radio-collars. Of these
flying squirrels, we conducted microhabitat surveys on 13 individuals (7 males, 6
females). We gathered a total of 802 telemetry locations (average = 62 ± 5 locations
per flying squirrel) for these 13 VNFS. Mean MCP home ranges were 4.2 ± 1.0 ha
(mean male MCP = 5.8 ± 1.6 ha, mean female = 2.3 ± 0.5 ha).
The 3 most-important explanatory habitat variables were organic soil horizon
depth, dominant overstory tree, and presence of understory Red Spruce. The mean
organic soil horizon depth was greater at telemetry points than at random points
(Table 1). Montane conifers were the dominant overstory trees at 73.5% of telemetry
points versus 57.7% of random points. Of the telemetry points with a dominant
hardwood overstory, 69.6% had some conifer component in the overstory and 4%
had Red Spruce regeneration present in the understory. Understory Red Spruce was
greater in random points than in telemetry points (Table 1), and Red Spruce regeneration
at random points occurred in both conifer- and hardwood-dominant plots
(48.5% and 9.2%, respectively). Other microhabitat variables (i.e., variables quantifying
ground cover and canopy cover) were not significantly different between
telemetry and random points (Table 1).
Species that occurred as the closest overstory tree included Red Spruce (25.8%
and 20% of telemetry and random points, respectively), Red Maple (25.0% and
29.2%), Yellow Birch (17.3% and 22.7%), Norway Spruce (11.9% and 6.5%),
Black Cherry (7.3% and 8.5%), American Beech (3.5% and 4.2%), Eastern Hemlock
(3.1% and 2.7%), and Betula lenta L. (Sweet Birch; 2.7% and 0.4%). Other
species documented at a small number of plots were Tilia americana L. (American
Table 1. Mean (± SE) and PerMANOVA results of microhabitat variables averaged across all individual
Glaucomys sabrinus fuscus (Virginia Northern Flying Squirrel) sample points, 2013–2014,
Allegheny Mountains, WV.
Telemetry Random F-statistic
Habitat vVariable plots plots (df = 1, 24) P
Organic matter depth (cm) 12.0 ± 1.3 8.6 ± 0.8 4.686 0.043
% bare ground 0.5 ± 0.4 0.7 ± 0.3 0.190 0.705
% moss cover 5.6 ± 1.4 5.2 ± 1.1 0.049 0.850
% duff cover 77.5 ± 2.6 74.9 ± 2.8 0.490 0.483
% woody debris 5.5 ± 0.5 4.7 ± 0.6 0.908 0.097
% herbaceous cover 11.0 ± 1.6 14.3 ± 2.4 1.362 0.350
% Canopy cover 76.4 ± 3.9 77.4 ± 2.3 0.050 0.838
Distance to closest overstory tree 2.2 ± 0.2 2.8 ± 0.3 3.302 0.080
Closest overstory tree (% plots with conifer) 40.8 ± 0.04 30.4 ± 0.04 3.388 0.066
Dominant overstory conifer (%) 73.5 ± 0.05 57.7 ± 0.06 4.105 0.048
Understory Red Spruce (% plots with regeneration) 22.3 ± 0.03 83.1 ± 0.07 59.040 less than 0.001
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Basswood), Pinus strobus L. (White Pine), Acer pensylvanicum L. (Striped Maple),
A. saccharum Marshall (Sugar Maple), Magnolia acuminata L. (Cucumber Magnolia),
and M. fraseri Walter (Fraser Magnolia). At telemetry points, the closest
overstory trees were 59.2% hardwood species and 40.8% conifer species. The
closest overstory trees at random points were 70.0% hardwood species and 29.2%
conifer species, and 0.8% of plots had no tree within 10 m of the plot center. The
average distance to closest tree was 2.2 m in telemetry points and 2.8 m in random
points, although this was not significantly dif ferent (Table 1).
Of the 260 telemetry points surveyed, we found hypogeal fungi digs and scratches
in 25.4% of the subplots and approximately half of those subplots contained
hypogeal fungi. We documented 3 species of hypogeal fungi: Elaphomyces americanum
Castellano, E. verruculosus Castellano, and E. macrosporus Castellano and
Trappe. We found the majority of digs during the spring seasons (86.4%), likely
because leaf deposition in mixed forests during the fall season made locating digs
difficult. Montane conifers were the closest overstory trees at 61.8% of plots where
hypogeal fungi were present, and all plots with hypogeal fungi had either Red
Spruce, Norway Spruce, or Eastern Hemlock as a dominant overstory tree (88.2%)
or these species were present in the midstory (11.8%). Soils were significantly
deeper at telemetry points with hypogeal fungi (mean = 12.5 ± 0.5) than telemetry
points without hypogeal fungi (8.6 ± 1.0; F259 = 8.888, P = 0.003).
Discussion
Small-mammal microhabitat studies typically obtain data from capture–no capture
sites in live-trapping grids (e.g., Jorgensen 2004, Meyer et al. 2007, Pyare and
Longland 2002, Rossell and Rossell 1999), but these data can be misleading because
baited-capture sites do not necessarily indicate microhabitat selection (Trainor et al.
2005), especially of foraging habitat. Although there is error associated with VHF
telemetry (White and Garrott 1990), we measured our error rate and corrected for
potential bias by using a larger plot size. The majority of the radio-collared individuals
were obtained from nest boxes placed along the conifer–northern hardwood
ecotone. Trapping and placing next boxes along the ecotone is associated with high
capture rates of Northern Flying Squirrels in the Appalachians (Hackett and Pagels
2003, Weigl et al. 1999); however, ecotonal habitat is more closely associated with
nesting habitat than foraging habitat (Diggins 2016, Ford et al. 2007, Loeb et al.
2000, Menzel et al. 2006). Our use of telemetry data reduced the bias effects of
baited-trap sites or selectively placed nest boxes on potential foraging habitat.
Macrohabitat conditions are typically considered better predictors of smallmammal
habitat selection than microhabitat characteristics (e.g., Coppeto et al.
2006, Morris 1987, Orrock et al. 2000) because microhabitat partitioning is usually
constrained by macrohabitat (Jorgensen and Demarais 1999). This limit may
be dependent on average home-range size of the species in question (e.g., Castleberry
et al. 2002). VNFS are highly mobile and can sometimes have home ranges
> 20 ha (Ford et al. 2007, Menzel et al. 2006); we found the majority of withinstand
habitat variables measured did not differ between selected and random sites.
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Canopy cover and herbaceous cover are known to influence Northern Flying
Squirrel microhabitat selection (Meyer et al. 2005, Pyare and Longland 2002,
Smith et al. 2004) because Northern Flying Squirrels may be more vulnerable to
predation in open stands (Carey et al. 1992). Urban (1988) found that fern cover
was positively correlated within VNFS core-activity areas versus low-activity
areas, whereas canopy cover was negatively correlated. However, neither variable
influenced microhabitat selection in our study. We posit that this finding is
explained by the fact that herbaceous cover was generally low at most sites we
surveyed (Table 1) and virtually absent from plots with hypogeal fungi. Canopy
cover was similar between telemetry and random points, regardless of whether
plots were dominated by hardwoods (75.1% ± 1.2 canopy cover) or montane conifers
(78.8% ± 0.9 canopy cover); thus, we detected no difference in overstory
cover between telemetry and random points.
Three habitat variables were significantly different between telemetry and
random plots: organic-soil horizon depth, dominant overstory tree, and presence
of understory Red Spruce. VNFS selected for deep organic-soil horizons that are
typically associated with conifer stands and may be linked to selection of hypogeal
fungi at foraging sites. Deeper organic-soil horizons also may be associated
with higher abundances of hypogeal fungi (Meyer et al. 2007), although we found
hypogeal fungi at telemetry points with shallower soils than telemetry points without
hypogeal fungi. Our exploration of hypogeal fungi was opportunistic and we
employed limited-time searches; thus, our searches for hypogeal fungi were incomplete
at most telemetry points, and further assessment needs to be made in regards
to soil depth and hypogeal fungi presence. Elaphomyces spp. occur in high proportions
in VNFS diets (Mitchell 2001). All 3 species of hypogeal fungi we found are
associated with Red Spruce or other conifers, such as Norway Spruce and Eastern
Hemlock (Castellano et al. 2012; M. Castellano, US Forest Service, Corvallis, OR,
pers. comm.). In a study of the Carolina Northern Flying Squirrel’s habitats in the
southern Appalachians, Red Spruce was considered the most important tree species
in plots with hypogeal fungi (Loeb et al. 2000). In our study, the majority of digs
(62%) were located within 2 m of a conifer, the zone near the host tree where most
hypogeal fungi occur (Fogel 1976). Presence of downed coarse woody debris is
considered an important indicator to flying squirrels for hypogeal fungi detection
(Pyare and Longland 2001), but coarse woody debris itself does not influence squirrel
occurrence (Meyer et al. 2007, Pyare and Longland 2002). We did not measure
coarse woody debris due to the low abundance observed throughout our study
sites. Although we only opportunistically sampled for hypogeal fungi, our success
in obtaining hypogeal fungi was much higher than a previous study on the VNFS
in the central Appalachians (Ford et al. 2004), likely because that study was based
on survey plots proximate to nest-box sites, which were not necessarily related to
foraging sites.
Similar to studies at the landscape and stand-level for Northern Flying Squirrels
in the central and southern Appalachians, we found that VNFS microhabitat selection
was linked to forests dominated by Red Spruce or other conifer surrogates
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(Ford et al. 2004, 2007, 2014; Menzel et al. 2004, 2005, 2006; Payne et al. 1989).
Pyare and Longland (2002) suggested that flying squirrel microhabitat selection
may be hierarchical, but our results indicate that presence of Red Spruce or a conifer
surrogate is more important in predicting microhabitat selection of VNFS
than other habitat features, such as herbaceous cover. Northern Flying Squirrel
home ranges are smaller in pure montane conifer stands than stands on the conifer–
northern hardwoods ecotone (Diggins and Ford, unpubl. data; Ford et al. 2014;
Menzel et al. 2006), suggesting that conifer stands have higher-quality habitat than
ecotonal stands. Menzel et al. (2006) found that radio-collared VNFS selectively
chose Red Spruce-dominant stands and mixed stands, and avoided pure northern
hardwood stands. Ford et al. (2014) and Diggins (2016) found that radio-collared
Carolina Northern Flying Squirrels selected Red Spruce more than expected based
on availability at both the between-stand level and within-stand level in the southern
Appalachians. Variation in microhabitat in Red Spruce stands, such as stand
maturity and tree condition, may influence the frequency of use at a site, but we did
not specifically address this question in the current study .
Understory Red Spruce was significantly lower at telemetry points versus random
points. Red Spruce regeneration, not herbaceous understory, was associated
with higher amounts of absolute understory cover, although we did not specifically
quantify density of regeneration over all of our study sites. In southeast Alaska,
Smith et al. (2004) found that conifer regeneration was lower at trap sites that
produced captures of flying squirrels than sites with no captures. However, other
research has indicated that increased understory vegetation might be important for
cover from predators, especially when foraging and handling food items (Longland
and Price 1991, Pyare and Longland 2002). Increased understory cover may also
hinder mobility on the ground (Carey 2000), which is considered a less-efficient
form of locomotion for flying squirrels (Scheibe et al. 2006). We found that Red
Spruce regeneration was significantly higher in random plots and hardwood dominated
forests. Microhabitat selection was not associated with hardwood-dominant
stands, regardless of the presence of Red Spruce regeneration in the understory.
Our findings link VNFS microhabitat selection to deep organic-soil horizons and
overstories comprised of montane conifer-dominated stands. Although adjacent
hardwood stands may provide denning opportunities (Hackett and Pagels 2003,
Menzel et al. 2004), our data suggest that conifer stands were more important foraging
habitat. The expansion of Red Spruce regeneration into adjacent hardwood
stands is indicative of ecological recovery of this forest type (Mayfield and Hicks
2010, Nowacki et al. 2010, Rollins et al. 2010), and should be a high priority for
restoration. Girdling, stem-injection herbiciding, or felling of hardwoods to mimic
natural canopy gaps (Rentch et al. 2010) would release single or small groups of
suppressed Red Spruce to the overstory and potentially provide a near-term increase
in potential den sites in newly created snags (Rentch et al. 2016). Although
Northern Flying Squirrels are sensitive to silvicultural treatments (Carey 2000,
Holloway and Smith 2011, Holloway et al. 2012), Red Spruce restoration occurs
on a relatively small scale within the forest compared to more common forestharvest
methods (i.e., clearcutting, green-tree retention). Restoration treatments
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C.A. Diggins and W.M. Ford
2017
185
are currently occurring in northern hardwood-dominant stands with suppressed Red
Spruce in the understory or midstory. The restoration treatments may not strongly
impact VNFS because they tend not to select these habitats. However, a better understanding
of VNFS response to Red Spruce restoration treatments is necessary to
understand short-term impacts of the treatments on this subspec ies.
Ours is the first microhabitat selection study of Northern Flying Squirrels in
the Appalachian Mountains and it may provide information pertinent to habitat
management of this subspecies. Denning habits of Northern Flying Squirrels in the
Appalachians may be plastic (Diggins et al. 2015, Hackett and Pagels 2003) and
foraging habitat could be a more important indicator of habitat occupancy of VNFS.
Red Spruce is predicted to decline in extent due to anthropogenic climate change,
potentially leading to the extirpation of this species from the central Appalachians
(Beane and Rentch 2015). Links to Red Spruce and other conifer surrogates on the
landscape-, stand-, and microhabitat-level should help managers prioritize areas for
habitat management and Red Spruce restoration to increase or retain as much of this
threatened habitat type as possible. Restoration will help increase the extent, connectivity,
and quality of the VNFS habitat, increasing the potential for population
persistence into an uncertain future climate within the central Appalachians.
Acknowledgments
We thank P. Curtin, L. Schablein, W. Thompson, K. Parker, and H.B. Hound for field assistance.
M. Castellano provided truffle identification. We are grateful to C. Stihler, S. Jones,
J. Wallace, R. Doyle, B. Sargent, E. Galford, J. Teets, M.B. Adams, J. Tribble, T. Kuntz, D.
Mitchell, S. Connelly, P. Weigl, D. Stauffer, K. Hennig, S. Karpanty, and M. Kelly. Housing
was provided by Snowshoe Ski Resort and Greenbrier Ranger District, Monongahela National
Forest. Funding was provided by the WV Division of Highways (Grant #T699-FLY/
SQ-1.00). Work was conducted under West Virginia Division of Natural Resources Scientific
Collecting Permit #2013.061 and #2014.033. Thanks to editor Tom French and 2 anonymous
reviewers, whose comments helped improve this manuscript.
Literature Cited
Allard, H.A., and E.C. Leonard. 1952. The Canaan and the Stony River Valleys of West
Virginia, their former magnificent spruce forests, their vegetation, and floristics today.
Castenea 17:1–60.
Amaranthus, M.P. 1998. The importance and conservation of ectomycorrizal fungal diversity
in forest ecosystems: Lessons from Europe and the Pacific Northwest. USDA Forest
Service General Technical Report PNW-GTR-431, Pacific Northwest Research Station,
Portland, OR. 15 pp.
Anderson, M.J. 2001. A new method for non-parametric multivariate analysis of variance.
Austral Ecology 26:32–46.
Beane, N.R., and J.S. Rentch. 2015. Using known occurrences to model suitable habitat
for a rare forest type in West Virginia under select climate change scenarios. Ecological
Restoration 33:178–189.
Byers, E.A., J.P. Vanderhorst, and B.P. Street. 2010. Classification and conservation assessment
of upland Red Spruce communities in West Virginia. West Virginia Natural
Heritage Program, WV Division of Natural Resources, Elkins, WV.
Northeastern Naturalist
186
C.A. Diggins and W.M. Ford
2017 Vol. 24, No. 2
Byers, E.A., K.C. Love, K.R. Haider, E.J. Burks, and J.E. Rowan. 2013. Red Spruce
(Picea rubens) cover in West Virginia. Version 1.0 West Virginia Division of Natural
Resources, Central Appalachian Spruce Restoration Initiative, Appalachian Forest Heritage
Area Americorps, Monongahela National Forest, and US Fish and Wildlife Service.
Available online at http://wvgis.wvu.edu/data/dataset.php?ID=455http://wvgis.wvu.
edu/data/dataset.php?ID=455. Accessed 17 March 2016.
Carey, A.B. 2000. Effects of new forest-management strategies on squirrel populations.
Ecological Applications 10:248–257.
Carey, A.B., S.P. Horton, and B.L. Biswell. 1992. Northern Spotted Owls: Influence of prey
base and landscape character. Ecological Monograph 62:223–250.
Castellano, M.A., J.E. Smith, T. O’Dell, E. Cázares, and Susan Nugent. 1999. Handbook
to Strategy- 1 Fungal Species in Northwest Forest Plan. USDA Forest Service General
Technical Report PNW-GTR-476. Pacific Northwest Research Station, Portland, OR.
205 pp.
Castellano, M.A., E. Cázares, B. Fondrock, and T. Dreisbach. 2003. Handbook to additional
fungal species of special concern in the Northwest Forest Plan. USDA Forest Service
General Technical Report PNW-GTR-572, Pacific Northwest Research Station, Portland,
OR. 81 pp.
Castellano, M.A., G.G. Guerrero, J.G. Jiménez, and J.M. Trappe. 2012. Elaphomyces appalachiensis
and E. verruculosus sp. Nov. (Ascomycota Eurotiales, Elaphomycetaceae)
from eastern North America. Revista Mexicana de Micologíca 35:17–22.
Castleberry, S.B., P.B. Wood, W.M. Ford, N.L. Castleberry, and M.T. Mengak. 2002. Summer
microhabitat selection of foraging Allegheny Woodrats (Neotoma magister) in a
managed forest. American Midland Naturalist 147:93–101.
Clarkson, R.B. 1964. Tumult on the Mountains: Lumbering in West Virginia: 1770–1920.
McClain Printing Company, Parsons, WV. 410 pp.
Coppeto, S.A., D.A. Kelt, D.H. Van Vuren, J.A. Wilson, and S. Bigelow. 2006. Habitat associations
of small mammals at two spatial scales in the northern Sierra Nevada. Journal
of Mammalogy 87:402–413.
Diggins, C.A. 2016. Determining habitat associations of Virginia and Carolina Northern
Flying Squirrels in the Appalachian Mountains from bioacoustic and telemetry surveys.
Ph.D. Dissertation. Virginia Polytechnic Institute and State University, Blacksburg, VA.
139 pp.
Diggins, C.A., C.A. Kelly, and W.M. Ford. 2015. Atypical den use of Carolina Northern
Flying Squirrels (Glaucomys sabrinus coloratus) in the southern Appalachian Mountains.
Southeastern Naturalist 14:N44–N49.
Dixon, P. 2003. VEGAN, a package of R functions for community ecology. Journal of
Vegetation Science 14:927–930.
Eager, C., and M.B. Adams (Eds.). 1992. Ecology and Decline of Red Spruce in the Eastern
United States. Springer-Verlag, New York, NY. 417 pp.
Ellison, A.M., M.S. Bank, B.D. Clinton, E.A. Colburn, K. Elliot, C.R. Ford, D.R. Foster,
B.D. Kloeppel, J.D. Knoepp, G.M. Lovett, J. Mohan, D.A. Orwig, N.L. Rodenhouse,
W.V. Sobczak, K.A. Stinson, J.A. Stone, C.M. Swan, J. Thompson, B. Von Holle, and
J.R. Webster. 2005. Loss of foundation species: Consequences for the structure and dynamics
of forested ecosystems. Frontiers in Ecology and the Environment 3(9):479–486.
Fenneman, N.M. 1938. Physiography of eastern United States. McGraw-Hill Book Company,
New York, NY. 714 pp.
Northeastern Naturalist Vol. 24, No. 2
C.A. Diggins and W.M. Ford
2017
187
Flegal, D.G. 1999. Soil Survey of Pocahontas County, West Virginia. US Department of
Agriculture, Natural Resources Conservation Service; in cooperation with the West Virginia
Agricultural and Forestry Experiment Station, Washington, DC. 299 pp.
Fogel, R. 1976. Ecological studies of hypogeous fungi. II. Sporocarp phenology in a western
Oregon Douglas Fir stand. Canadian Journal of Botany 54:1 152–1162.
Fogel, R., and J.M. Trappe. 1978. Fungus consumption (mycophagy) by small animals.
Northwest Science 52:1–31.
Ford, W.M., S.L. Stephenson, J.M. Menzel, D.R. Black, and J.W. Edwards. 2004. Habitat
characteristics of the endangered Virginia Northern Flying Squirrel (Glaucomys
sabrinus fuscus) in the central Appalachian Mountains. American Midland Naturalist
152:430–-438.
Ford, W.M., K.N. Mertz, J.M. Menzel, and K.K. Sturm. 2007. Winter home range and habitat
use of the Virginia Northern Flying Squirrel (Glaucomys sabrinus fuscus). USDA
Forest Service Research Paper NRS-4, Northern Research Station, Newtown Square,
PA. 16 pp.
Ford, W.M., K.R. Moseley, C.W. Stihler, and J.W. Edwards. 2010. Area occupancy and
detection probabilities of the Virginia Nnorthern Fflying Ssquirrel (Glaucomys sabrinus
fuscus) using nest-box surveys. Pp. 39–-47, In , J.S. Rentch and T.M. Schuler (Eds.).
Proceedings from the conference on the ecology and management of high-elevation forests
in the central and southern Appalachian Mountains. Rentch, J.S., and T.M. Schuler
(Eds.). USDA Forest Service General Technical Report NRS-P-64, Northern Research
Station, Newtown Square, PA. 242 pp.
Ford, W.M., C.A. Kelly, J.L. Rodrigue, R.H. Odom, D. Newcomb, L.M. Gilley, and C.A.
Diggins. 2014. Late winter and early spring home range and habitat use of the endangered
Carolina Northern Flying Squirrel in western North Carolina. Endangered Species
Research 23:73–-82.
Ford, W.M., A.M. Evans, R.H. Odom, J.L. Rodrigue, C.A. Kelly, N. Abaid, C.A. Diggins,
and D. Newcomb. 2015. Predictive habitat-models derived from nest-box occupancy for
the endangered Carolina Northern Flying Squirrel in the southern Appalachians. Endangered
Species Research 27:13–140.
Getz, W.M., and C.C. Wilmers. 2004. A local nearest-neighbor convex-hull construction of
home ranges and utilization distributions. Ecography 27:489–505 .
Hackett, H.M., and J.F. Pagels. 2003. Nest-site characteristics of the endangered Northern
Flying Squirrel (Glaucomys sabrinus coloratus) in southwest Virginia. American Midland
Naturalist 150:321–331.
Harley, J.L., and S.E. Smith. 1983. Mycorrhizal symbiosis. Academic Press, London, UK.
500 pp.
Holloway, G.L., and W.P. Smith. 2011. A meta-analysis of forest age and structure effects on
Northern Flying Squirrel densities. Journal Wildland Management 75:668–674.
Holloway, G.L., W.P. Smith, C.B. Halpern, R.A. Gitzen, C.C. Maguire, and S.D. West.
2012. Influence of forest structure and experimental green-tree retention on Northern
Flying Squirrel (Glaucomys sabrinus) abundance. Forest Ecology and Management
285:187–194.
Johnson, C.N. 1996. Interactions between mammals and ectomycorrhizal fungi. Trends in
Ecology and Evolution 11:503–507.
Jorgensen, E.E. 2004. Small-mammal use of microhabitat reviewed. Journal of Mammalogy
85:531–539.
Jorgensen, E.E., and S. Demarais. 1999. Spatial-scale dependence of rodent habitat use.
Journal of Mammalogy 80:421–429.
Northeastern Naturalist
188
C.A. Diggins and W.M. Ford
2017 Vol. 24, No. 2
Koprowski, J.L., S.R.B. King, and M.J. Merrick. 2008. Expanded home ranges in a peripheral
population: Space use by endangered Mt. Graham Red Squirrels. Endangered
Species Research 4:227–232.
Korstian, C.F. 1937. Perpetuation of spruce on cut-over and burned lands in the higher
Southern Appalachian Mountains. Ecological Monographs 7:125–167.
Loeb, S.C., G.L. Chapman, and T.R. Ridley. 1999. Sampling small mammals in southeastern
forests: The importance of trapping in trees. Proceedings of the Annual Conference
of the Southeastern Associated Fish and Wildlife Agencies 53:415–424.
Loeb, S.C., F.H. Tainter, and E. Cazares. 2000. Habitat associations of hypogeous fungi in
the southern Appalachians: Implications for the endangered Northern Flying Squirrel
(Glaucomys sabrinus coloratus). American Midland Naturalist 144:286–296.
Longland, W.S., and M.V. Price. 1991. Direct observations of owls and heteromyid rodents:
Can predation explain microhabitat use. Ecology 72:2261–2273.
Maser, C., J.M. Trappe, and R.A. Nussbaum. 1978. Fungal–small mammal interrelationships
with emphasis on Oregon coniferous forests. Ecology 59:799–809.
Maser, C., A.W. Claridge, and J.M. Trappe. 2008. Trees, Truffles, and Beasts: How Forests
Function. Rutgers University Press, New Brunswick, NJ. 288 pp.
Maser, Z., C. Maser, and J.M. Trappe. 1985. Food habits of the Northern Flying Squirrel
(Glaucomys sabrinus) in Oregon. Canadian Journal of Zoology 63:1084–1088.
Mayfield, A.E., and R.R. Hicks. 2010. Abundance of Red Spruce regeneration across
spruce–hardwood ecotones at Gaudineer Knob, West Virginia. Pp. 113–125, In J.S.
Rentch and T.M. Schuler (Eds.). Proceedings from the conference on the ecology and
management of high-elevation forests in the central and southern Appalachian Mountains.
USDA Forest Service General Technical Report NRS-P-64. Northern Research
Station, Newtown Square, PA. 242 pp.
Menzel, J.M., W.M. Ford, J.W. Edwards, and M.A. Menzel. 2004. Nest-tree use by the
endangered Virginia Northern Flying Squirrel in the central Appalachian Mountains.
American Midland Naturalist 151:355–368.
Menzel, J.M., W.M. Ford, J.W. Edwards, and L.J. Ceperley. 2005. A habitat model for the
Virginia Northern Flying Squirrel (Glaucomys sabrinus fuscus) in the central Appalachian
Mountains. USDA Forest Service Research Paper NE-729. Northeastern Research
Station, Newtown Square, PA. 14 pp.
Menzel, J.M., W.M. Ford, J.W. Edwards, and T.M. Terry. 2006. Home range and habitat use
of the vulnerable Virginia Northern Flying Squirrel Glaucomys sabrinus fuscus in the
central Appalachian Mountains, USA. Oryx 40:204–210.
Meyer, M.D., M.P. North, and D.A. Kelt. 2005. Fungi in the diets of Northern Flying
Squirrels and Lodgepole Chipmunks in the Sierra Nevada. Canadian Journal of Zoology
83:1581–1589.
Meyer, M.D., D.A. Kelt, and M.P. North. 2007. Microhabitat associations of Northern Flying
Squirrel in burned and thinned forest stands of the Sierra Nevada. American Midland
Naturalist 157:202–211.
Mitchell, D. 2001. Spring and fall diet of the endangered West Virginia Northern Flying
Squirrel (Glaucomys sabrinus fuscus). American Midland Naturalist 146:439–443.
Mitchell, M.S., and R.A. Powell. 2008. Estimated home ranges can misrepresent habitat
relationships on patch landscapes. Ecological Modelling 216:409 –414.
Morris, D.W. 1987. Ecological scale and habitat use. Ecology 68:362–369.
Nauman, T.W., J.A. Thompson, S.J. Teets, T.A. Dilliplane, J.W. Bell, S.J. Connolly, H.J.
Liebermann, and K.M. Yoast. 2015. Ghosts of the forest: Mapping pedomemory to guide
forest restoration. Geoderma 247–248:51–64.
Northeastern Naturalist Vol. 24, No. 2
C.A. Diggins and W.M. Ford
2017
189
Newins, H.S. 1931. Forest conditions of West Virginia. Journal of Forestry 29:565–571.
Noss, R.F., E.T. LaRoe, and J.M. Scott. 1995. Endangered ecosystems of the United States:
A preliminary assessment of loss and degradation. Biological Report 28. US National
Biological Service, Washington, DC. 95 pp.
Nowacki, G., R. Carr, and M. Van Dyck. 2010. The current status of Red Spruce in the
Eastern United States: Distribution, population trends, and environmental drivers. Pp.
14–162, In J.S. Rentch, and T.M. Schuler (Eds.). Proceedings from the conference on
the ecology and management of high-elevation forests in the central and southern Appalachian
Mountains USDA Forest Service General Technical Report NRS-P-64, Northern
Research Station, Newtown Square, PA. 242 pp.
Odom, R.H., W.M. Ford, J.W. Edwards, C.W. Stihler, and J.M. Menzel. 2001. Developing
a habitat model for the endangered Virginia Northern Flying Squirrel (Glaucomys
sabrinus fuscus) in the Allegheny Mountains of West Virginia. Biological Conservation
99:245–252.
Oksanen, J., R. Kindt, P. Legendre, B. O’Hara, G.L. Simpson, P. Solymos, M. Henry, H.
Stevens, and H. Wagner. 2009. The vegan package. Available online at http://vegan.rforge.
r-project.org. Accessed 31 March 2014.
Orrock, J.L., and J.F. Pagels. 2002. Fungus consumption by the Southern Red-backed Vole
(Clethrionomys gapperi) in the Southern Appalachians. American Midland Naturalist
147:413–418.
Orrock, J.L., J.F. Pagels, W.J. McShea, and E.K. Harper. 2000. Predicting presence and
abundance of a small-mammal species: The effect of scale and resolution. Ecological
Applications 10:1356–1366.
Payne, J.L., D.R. Young, and J.F. Pagels. 1989. Plant-community characteristics associated
with the endangered Northern Flying Squirrel, Glaucomys sabrinus, in the southern Appalachians.
American Midland Naturalist 121:285–292.
Pyare, S., and W.S. Longland. 2001. Mechanisms of truffle detection by Northern Flying
Squirrels. Canadian Journal of Zoology 79:1007–1015.
Pyare, S., and W.S. Longland. 2002. Interrelationships among Northern Flying Squirrels,
truffles, and microhabitat structure in Sierra Nevada old-growth habitat. Canadian Journal
of Forest Research 32:1016–1024.
Pyle, R.E., W.W. Beverage, T. Yoakum, D.P. Amick, W.F. Hatfield, and D.E. McKinney.
1982. Soil Survey of Randolph County Area Main Part, West Virginia. US Department
of Agriculture, Natural Resources Conservation Service; in cooperation with the West
Virginia Agricultural and Forestry Experiment Station, Washington, DC. 181 pp.
R Core Development Team. 2015. R: A Language and Environment for Statistical Computing,
Vienna, Austria.
Rentch, J.S., T.M. Schuler, W.M. Ford, and G.J. Nowacki. 2007. Red Spruce stand dynamics,
simulations, and restoration opportunities in the central Appalachians. Restoration
Ecology 15:440–-452.
Rentch, J.S., T.M. Schuler, G.J. Nowacki, N.R. Beane, and W.M. Ford. 2010. Canopy- gap
dynamics of second-growth Red Spruce–-northern hardwood stands in West Virginia.
Forest Ecology and Management 260:1921–1929.
Rentch, J.S., W.M. Ford, T.S. Schuler, J. Palmer, and C.A. Diggins. 2016. Release of suppressed
Red Spruce using canopy-gap creation: Testing applicability for ecological
restoration in the Central Appalachians. Natural Areas Journal 36:500–508.
Reynolds, R.J., J.F. Pagels, and M.L. Fies. 1999. Demography of Northern Flying Squirrels
in Virginia. Proceedings of the Annual Conference of the Southeastern Association of
Fish and Wildlife Agencies 53:340–349.
Northeastern Naturalist
190
C.A. Diggins and W.M. Ford
2017 Vol. 24, No. 2
Rollins, A.W., H.S. Adams, and S.L. Stephenson. 2010. Changes in forest composition and
structure across the Red Spruce–hardwood ecotone in the central Appalachians. Castanea
75:303–314.
Rossell, C.R., and I.M. Rossell. 1999. Microhabitat selection by small mammals in a southern
Appalachian fen in the USA. Wetland Ecology and Management 7:219–224.
Scheibe, J.S., W.P. Smith, J. Bassham, and D. Magness. 2006. Locomotor performance and
cost of transport in the Northern Flying Squirrel, Glaucomys sabrinus. Acta Theriologica
51:169–178.
Schmutz, J.A., and G.C. White. 1990. Error in telemetry studies: Effect of animal movement
on triangulation. Journal of Wildlife Management 54:506–510.
Schuler, T.M., W.M. Ford, and R.J. Collins. 2002. Successional dynamics and restoration
implications of a montane coniferous forest in the central Appalachians, USA. Natural
Areas Journal 22:88–98.
Shanley, C.S., S. Pyare, and W.P. Smith. 2013. Response of an ecological indicator to landscape
composition and structure: Implications for function units of temperate rainforest
ecosystem. Ecological Indicators 24:68–74.
Smith, G.F., and N.S. Nicholas. 1999. Post-disturbance spruce–fir forest-stand dynamics at
seven disjunct sites. Castanea 64:175–186.
Smith, W.P., S.M. Gende, and J.V. Nicholas. 2004. Ecological correlates of flying squirrel
microhabitat use and density in temperate rainforests of southeastern Alaska. Journal of
Mammalogy 85:663–674.
Stephenson, S.L. 1993. Upland forests of West Virginia. McClain Printing Company, Parsons,
WV. 295 pp.
Stihler, C.W., K.B. Knight, and V.K. Urban. 1987. The Northern Flying Squirrel in West
Virginia. Pp. 176–183, In R.R. Odum, K.A. Riddleberger, and J.C. Dozier (Eds.). Proceedings
of 3rd Southeast Nongame and Endangered Species Symposium. University of
Georgia, Athens, GA. 253 pp.
Stihler, C.W., J.L. Wallace, E.D Michael, and H. Pawelczyk. 1995. Range of Glaucomys
sabrinus fuscus, a federally endangered subspecies of the Northern Flying Squirrel in
West Virginia. Proceedings of the West Virginia Academy of Science 67:13–20.
Trainor, A.M., T.M. Shenk, and K.R. Wilson. 2005. Microhabitat characteristics of Preble’s
Jumping Mouse high-use areas. Journal of Wildlife Management 71:469–477.
Urban, V. 1988. Home range, habitat utilization, and activity of the endangered Northern
Flying Squirrel. M.Sc. Thesis. West Virginia University, Morgantown, WV. 59 pp.
US Fish and Wildlife Service (USFWS). 1985. Final rule for listing Carolina Flying Squirrel
and Virginia Flying Squirrel as endangered. 50 Federal Register:27002. Washington, DC.
USFWS. 2013. Endangered and threatened wildlife and plants: Reinstatement of removal
of the Virginia Northern Flying Squirrel from the list of Endangered and Threatened
wildlife. 78 Federal Register:14022. Washington, DC.
Weigl, P.D., T.W. Knowles, and A.C. Boynton. 1999. The distribution and ecology of the
Northern Flying Squirrel, Glaucomys sabrinus coloratus, in the southern Appalachians.
North Carolina Wildlife Resources Commission Publication, Raleigh, NC. 93 pp.
Wells-Gosling, N., and L.R. Heaney. 1984. Glaucomys sabrinus. Mammalian Species
229:1–8.
White, G.C. 1985. Optimal locations of towers for triangulation studies using biotelemetry.
Journal of Wildlife Management 49:190–196.
White, G.C., and R.A. Garrott. 1990. Analysis of wildlife radio-tracking data. Academic
Press, New York, NY. 383 pp.
White, P.S., M.D. MacKenzie, and R.T. Busing. 1985. A critique on overstory/understory
comparisons based on transition-probability analysis of an old-growth spruce–fir stand
in the Appalachians. Vegetatio 64:37–45.