Interna tional Journal of Forest, Animal and Fisheries Research (IJFAF)
https://dx.doi.org/10.22161/ijfaf.2.2.2
[Vol-2, Issue-2, Mar-Apr, 2018]
ISSN: 2456-8791
The influence of the foodscape on quaking aspen
stand condition and use by ungulates
Kristen Y. Heroy1,2*, Samuel B. St. Clair3, Paul C. Rogers1,2,4, Juan J. Villalba1,2
1
Department of Wild and Resources, Utah State University, Logan 84322, USA
2
Ecology center, Utah State University, Logan, UT 84322-5205, USA
3
Department of Plant & Wildlife Sciences, Brigham Young University, Provo, UT, 84602 USA
4
Western Aspen Alliance
*
e-mail:
[email protected], Tel: 435-797-3576, Fax: 435-797-3796
Abstract— In order to study the effects of herbivory on
plant communities, we determined whether the types and
concentrations of chemicals present in different aspen
(Populus tremuloides Michx.) stands and understories,
i.e., the foodscape, are associated with aspen use by elk
(Cervus elaphus L.) and with aspen regeneration and
recruitment. Transects were established in aspen stands
with high, medium, and low regeneration levels (N=5
locations/regeneration level; ranging from 2,331 m to
2,724 m in elevation) in Wolf Creek Ranch in northern
Utah. Using non-metric multidimensional scaling
(NMDS) ordination and regression analyses, we
examined the relationships between aspen regeneration,
recruitment, elk presence, browsing, and other landscape
elements with the foodscape (e.g., biomass and chemical
composition of the understory and chemical defenses of
juvenile aspen trees). The foodscape was affected by
elevation and canopy height but it did not explain aspen
use or indicators of aspen resilience. Our findings
suggest that foodscapes of lower nutrient content–
occurring at lower elevations under drier climatic
conditions–are more likely to foster aspen stands with
less forb and grass understory, and thus lower nutritional
biomass. Nevertheless, the extent of the decline in the
availability of nutrients in the understory did not appear
to influence aspen browsing or indicators of aspen
resilience. Future research should focus on exploring the
influence of additional–and more contrasting–gradients
of chemical availability in the landscape on aspen use by
herbivores.
Keywords— Browsing, Elk, Phenolic glycosides, Plant
secondary compounds, Preference.
I.
INTRODUCTION
Landscapes offer herbivores a diversity of types and
concentrations of chemicals (i.e., the foodscape)
packaged inside an array of forage species distributed
across different temporal and spatial scales [1-6]. In turn,
foraging decisions by herbivores are influenced by the
heterogeneous distribution of chemicals in time and
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space, relative to the type of animal and its history with
the foodscape [7-11]. In addition to the distribution of
chemicals, foraging choices are driven by other biotic
(e.g., perceived likelihood of predation, human presence,
hunting, co-grazing) and physiographic (e.g., elevation,
climate, slope) factors, which further influence animal
movement and grazing patterns across plant communities
[7,12,13].
Aspen (Populus tremuloides Michx.) communities
represent an ideal study system to explore the influence of
the foodscape on foraging decisions by herbivores
because they provide a wide variety of plant diversity to
consumers [14-16], and because aspen trees show
substantial genetically-based variation in phytochemical
traits that influence foraging behavior [17]. Despite this
diversity and presence of chemical defenses, repeated
foliage removal and damage to meristematic tissues from
herbivory continue to impact aspen trees to the point of
representing a major cause of poor aspen regeneration in
some areas of North America [18] and Eurasia [19].
Herbivores are sensitive to changes in the nutritional
quality of plants in a community; they modify their
dietary breadth as well as the amounts and proportions of
ingested plant parts and species in order to meet their
nutritional needs [e.g., 20,21]. This is why wild and
domestic ungulates typically prefer aspen in the fall,
when the average nutritional quality offered by the
understory drops below that present in aspen tissues
[16,22,23]. Additionally, studies with sheep have revealed
that aspen intake is dependent on the types of feed an
animal has recently consumed [5], as well as on the
animals’ nutritional state [5,6]. For instance, ingesting
foods containing high concentrations of protein enhances
aspen intake, especially if plant defenses in aspen are
present in low concentrations [5,6]. On the other hand,
because aspen is a good source of starch, energyrestricted sheep consume greater amounts of aspen leaves
than control (i.e., non-restricted) animals [6].
Herbivores also respond to plant secondary compounds
(PSC) by reducing the amount of PSC-containing plants
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that they consume [24], a process regulated by the
complementarities and antagonisms occurring across
different detoxification pathways and the availability of
nutrients needed for detoxification processes [24-26].
Aspen chemical defenses (phenolic glycosides and
condensed tannins) have been shown to deter ungulate
browsing, but when ungulate numbers increase above a
certain threshold, the capacity of these defenses to deter
browsing to a level that effectively restricts tissue loss to
herbivores gets compromised [reviewed by 27]).
Consistent with this idea, a recent study conducted at the
same location where the present study was carried out
reports that a majority of the aspen stands assessed were
not recruiting new stems at sufficient levels to replace
overstory trees [28]. This response was likely a
consequence of elk numbers exceeding the carrying
capacity desired by managers for the region [28], which
was estimated to be below one animal km-2 [29,30].
Nevertheless, Rogers et al. (2015) [28] did not determine
the types and amounts of nutrients provided by the
surrounding understory or the chemical composition of
aspen trees in that region.
Collectively, it follows that chemicals present in aspen, as
well as those offered by the surrounding vegetation, shape
herbivores’ decisions on how much aspen will be
incorporated into their diet. Thus, identifying the
concentration of different nutrients and PSC across the
landscape, i.e. the geospatial variation in the quality of
food or “foodscape,” is critical for understanding
herbivores’ preferences in diverse plant communities like
those observed in aspen-dominated landscapes [4,31].
The objective of this study was to characterize the
chemical composition of different aspen and
accompanying understory communities across a gradient
of aspen recruitment in order to determine whether the
types and concentrations of nutrients and PSC in the
landscape (i.e., the foodscape) are associated with aspen
use by elk and with aspen regeneration and recruitment.
We hypothesized that nutrients in juvenile aspen and the
surrounding vegetation interact with plant secondary
compounds to influence aspen use by herbivores. Thus,
we predicted that (i) as nutritional biomass in the
understory increased (i.e., greater amounts of crude
protein), aspen use would decrease and recruitment
(number of stems reaching > 2 m in height) and
regeneration (number of stems growing to ≤ 2 m in
height) would increase because herbivores would prefer
an understory with greater amounts and concentrations of
nutrients over defended aspen tissue. Additionally, we
predicted that (ii) as defense content in aspen stands
increased, aspen use would decrease because
phytochemicals constrain food intake. If our predictions
are true, aspen in areas with high understory biomass
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would experience less browsing, especially if they
contained high concentrations of defense compounds.
However, if the surrounding understory contains low
understory biomass, then aspen herbivory would be less
constrained by such defenses and aspen intake would
increase because those animals would be more willing to
consume defended foliage in order to meet nutritional
requirements. This means that stands with low understory
biomass may be more at risk of succumbing to herbivory
pressure and would need more intensive management
than stands with greater understory biomass.
II.
MATERIALS AND METHODS
2.1 Study site
Wolf Creek Ranch (WCR) is located east of Park City,
UT, USA (N 40° 30.6365’ W 111° 14.673’), and is
situated on a 5,382 hectare private parcel of land, with
approximately 2,333 hectares (~43% of the property)
covered by aspen forests that consist of a stable aspen
community-topped plateau that borders public land to the
east and private land on all other sides [28,32]. Loamy
soils dominate WCR, and surface soils primarily overlay
Keetley volcanic tuffs and resemble those soils found in
forested areas within this region [28]. Although most of
the aspen within WCR are found between 1,950 and
2,443 m of elevation, the property ranges from 1,950 to
2,750 m of elevation. The average precipitation at WCR
is 694 mm (measured from 1987 to 2012 using the nearest
rain gauge; SNOTEL #330), most of which occurs in the
form of snow during the winter season, and with midsummer being the driest period of the year [28].
Because elevation is variable within WCR, aspen
phenology, morphology, and community composition
varies markedly across the property [33]. Locations at
lower elevations tend to be drier and contain aspen and
conifer forests among areas of mountain big sagebrush
(Artemisia tridentata ssp. vaseyana Rydb.) or bigtooth
maple (Acer grandidentatum Nutt.) and Gambel oak
(Quercus gambelii Nutt.). Wetter locations at higher
elevations are dominated by stable aspen stands (singlespecies stands with little to no competition with conifers;
also called “pure” aspen stands) [32,34,35] with some
conifer cover (mainly Douglas-fir [Pseudotsuga menziesii
Franco], subalpine fir [Abies lasiocarpa Nutt.], and white
fir [Abies concolor Lindl. ex Hildebr.]) on north- and
east-facing slopes [28].
Herbivores within WCR are primarily mule deer
(Odocoileus hemionus Raf.), rocky mountain elk (Cervus
elaphus L.), and sheep (Ovis spp.), although moose (Alces
alces) are occasionally spotted in the area. Elk numbers
were estimated to be moderate-to-high for the habitat
found in WCR. Deer numbers are not well known on the
property [28]. Hunting is not typically permitted on
WCR, but a small number of guided elk hunting permits
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were issued in 2013. Hunting is allowed on adjacent
National Forest and private properties to the west, north,
and east of WCR. This proximity of hunted lands to
privately restricted lands increases elk numbers
seasonally as animals flee to safer zones. Property
managers in WCR allow 3,000 sheep to graze for two
weeks each year in June and six to seven weeks in
October and November. Although sheepherders are
instructed to keep sheep out of aspen stands to reduce
aspen browsing, browsing sometimes occurs [28].
2.2 Preceding study
In a preceding study completed by Rogers et al. (2015)
[28], the authors identified fifty random sample points
from an overlaid grid and aspen cover layer using a GIS
program. Seven of the locations were eliminated because
aspen cover was less than 50% tree cover. Within the
forty-three remaining locations, a 1-ha monitoring plot
was established within each location. Within each plot,
forest structure, tree composition, regeneration,
recruitment, landscape elements, percent of browsed
aspen, and herbivore use was measured. Tree diameters
and heights were converted to estimates or classifications
to accommodate non-expert field technicians. The data
were collected by trained citizen scientists during June
and July of 2012.
Measurements within 1-ha monitoring plots were
completed within two 2 m x 30 m belt transects oriented
perpendicular to each other at cardinal directions to
capture differences in terrain. Aspen regeneration
(number of stems < 2 m tall), recruitment (number of
stems ≥ 2 m and ≤ 6 m tall), and mature canopy trees
(trees > 6m tall) were determined within transects at each
location. Average canopy height was estimated for the
tallest layer of trees using a Biltmore stick. In addition,
the number of distinct fecal piles within the transects
were counted [36], and separated by species for mule
deer, elk, and sheep. Fecal piles that could not be
positively identified were not counted, and the frequency
of these incidences was not noted. Mean values from
variables measured within transects were assumed to
represent the surrounding 1-ha area and were extrapolated
from the area of the transects (120 m2) to 1-ha values (x
83.33) [28].
Rogers et al. (2015) [28] found that 46% of the stands
analyzed were not self-replacing and 19% were
marginally self-replacing using regeneration standards
provided in O’Brien et al. (2010) [37]. Using browse
thresholds for regeneration sustainability presented in
Jones et al. (2005) [38], 72% of the stands sampled did
not reach the recruitment threshold for long-term
sustainability of the stand. The majority of counted fecal
pellet piles within the entire 43 locations sampled
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corresponded to elk (96 elk fecal piles, 8 deer fecal piles,
0 sheep fecal piles), and populations were estimated to
occur in a density of 7.8 elk km-2. Previous studies
concluded that elk presence of < 1 elk km-2 was ideal for
successful stand-replacing recruitment [29,30]. Rogers et
al. (2015) [28] also found there was a negative
relationship between elk presence (estimated via pellet
counts) and aspen regeneration and recruitment. The same
areas with high elk pellets also had poor regeneration,
recruitment, and stand conditions. Elk presence did not
show a relationship with slope however, in agreement
with Rogers and Mittanck (2014) [39]. Hill aspect had a
positive relationship with recruitment and a negative
relationship with elk presence. Elk seemed to prefer drier
aspects and browse impacts were greater in these areas, or
fecal pellets were easier to find in the less densely
covered understory.
2.3 Foodscape Assessment
Fifteen locations were chosen from the forty-three
locations studied by Rogers et al. (2015) [28]. We chose
fifteen stands because of sampling logistics and because
five stands of each treatment was expected to provide
enough power to detect differences across locations. Five
high, medium, and low recruitment TPA (recruitment as a
percentage of live mature aspen trees per area) locations
were chosen to be surveyed and sampled, ranging in
elevation from 2,331 m to 2,724 m (see Fig 1 for
locations of aspen stands sampled). All locations were
under different levels of browsing pressure and thus no
Control area (i.e., no browsing) could be used in the
study. The cut-offs for high, medium, and low
recruitment TPA were developed by Rogers et al. (2015)
[28] based on the ability of the aspen stand to replace
itself over time under varying levels of herbivory. Stands
were selected so that one stand from each recruitment
TPA level was located within a distance of 1.5 km of each
other in order to minimize variation in environmental
conditions across the stands. Factors that disqualified
locations were slopes greater than 20° (given constraints
with site access), areas completely defoliated by aspen
blight, and locations that were less than 100 m from a
paved road or human structure.
Measurements within 1 ha monitoring plots were
completed within two 1 m x 30 m belt transects oriented
perpendicular to each other at cardinal directions to
capture terrain variations according to the methods of
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Fig.1: Locations of high, medium, and low regeneration
aspen stands (five of each regeneration level to total
fifteen stands) sampled during the study at the Wolf Creek
Ranch (WCR).
The location of WCR within Utah is shown in the inlaid
map of Utah in the upper right corner.
Rogers et al. (2015) [28]. Forage samples were taken
every 5 m on alternating sides of the belt transect using a
0.1 m2 quadrat sampling square, so that twelve samples
(all herbaceous plants at ground cover) were taken for
each location and placed in separate paper bags. Sampling
occurred during six consecutive days from 24-Aug-2015
to 29-Aug-2015, since browsing ungulates appear to
consume greater amounts of aspen in the early fall [40].
We acknowledge the three-year gap between the original
aspen forest data collected by Rogers et al. (2015) [28]
and the chemical composition of the foodscape reported
here. Nevertheless, very small-to-no-change in
recruitment and very small changes in regeneration are
expected under that time frame when aspen stands are
under the influence of herbivory as the major agent of
disturbance [41,42].
To assess shrub density and abundance, the length and
width of all shrubs within the 1 m x 30 m belts were
recorded [43,44]. In addition, a reference branch was
chosen from a shrub of the same species that lay outside
of the transects, which was used to estimate the leaf
biomass of the shrubs within the lanes, using the
reference unit method [45]. Briefly, leaf biomass was
estimated by holding up the reference branch to the shrub
in the 1 m x 30 m lane and approximating how many
reference branches fit inside the shrub in the lane. The
reference branch leaf biomass–later measured in the lab–
was then multiplied by this number in order to estimate
the leaf biomass on each shrub [45]. Reference branches
were replaced at least once per day and leaves were
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stripped off the branch and placed into an individual
paper bag, or sooner if leaves began to dry out because
the reference branch leaves had to be intact for accurate
estimations of dry matter. Mean values of variables
measured within transects and quadrats were extrapolated
to represent the surrounding 1-ha area. Shrub leaf weight
was extrapolated from the area of the transects (60 m2) to
1-ha values (× 166.66).
In order to determine food type biomass, weights of all
twelve clip samples were summed, then divided by 1.2
m2 to determine average weight (kg) of samples in 1 m2,
and then converted to kg ha-1 (× 10,000). All forage
weights were expressed as kg DM ha-1. The nutritional
constituent biomass (i.e., the amount of nutrients
available per unit of area) was calculated by the product
of the forage biomass and the concentration of nutrients
in the forages (e.g., i.e., kg crude protein ha -1, kg fiber
ha -1).
Aspen leaf samples were taken from each location from
trees with an approximate maximum height of 2 to 2.5 m,
when possible, by stripping leaves from no more than two
branches per aspen tree and placing them into paper bags.
The range of 2 to 2.5 m was chosen because trees at or
below this height are below the browse line and
consequently used by large ungulates like elk [46]. A
minimum of 25 g of leaves were harvested from each
stand by collecting leaves from each tree within a 30 m
radius of the center of the transect. If a location did not
contain any aspen trees between 2 to 2.5 m within the 30
m radius, then trees closest in height to 2 to 2.5 m were
used. Stand number and tree height for the stands that did
not contain any aspen trees within the selected height
range were: stand 9 (high regeneration stand; ~3 m in
height), stand 6 (medium regeneration; < 1 m in height),
and stand 7 (low regeneration stand; ~3 m in height).
We utilized information gathered by Rogers et al. (2015)
[28] (e.g., recruitment stems ha-1, regeneration stems ha1, recruitment TPA, live aspen stems ha-1, percent aspen
cover, canopy height, percent of aspen browsed,
elevation, slope, and aspect) from the fifteen sampled
stands to determine their relationship with the foodscape
(i.e., understory food type biomass, understory nutrient
constituent biomass, aspen defense chemistry) assessed in
the present study (see Table 1 for variables assessed in
Rogers et al. [2015] [28] and variables assessed in the
current study).
2.4 Forage analyses
All understory, shrub, and aspen leaf samples were stored
at -20 °C within 60 minutes of sample collection. Frozen
samples were transported in coolers to Utah State
University in Logan, UT and stored in a freezer upon
arrival. Freeze drying was used instead of oven-drying to
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better preserve the chemical composition of plant samples
[47]. All aspen and understory samples were kept at -20
°C until they were freeze-dried. Samples were weighed
before and after freeze-drying in order to determine dry
matter content.
Table.1: Variables used in the study.
Variables assessed by Rogers et al. 2015:
Regeneration stems ha-1
Recruitment stems ha-1
Recruitment TPA percentage
Landscape (physiographic) elements
Elevationf
Slope
Aspect
Percent browsed aspen
Fecal pellet counts
Percent aspen canopy cover
Canopy height
Variables assessed during the current study:
Aspen leaf chemistryg
CPa, ADFb, NDFc, TDNd, Tremulacin,
Salicortin, Total PG, Condensed tannins
Understory food type biomasse
Grass, Forb, Dead material, Shrubs
Nutrients within each understory food typee
CPa, ADFb, NDFc, Hemicellulose, TDNd
Total understory nutrients within each locatione
CPa, ADFb, NDFc, Hemicellulose, TDNd
Total understory biomass within each locatione
a
Crude protein
Acid detergent fiber
c
Neutral detergent fiber
d
Total digestible nutrients
e
Kg ha-1 on a dry matter basis
f
Meters
g
Percent of dry matter
b
2.5 Forage separation
After drying, each forage sample obtained from the
quadrats was separated into three food types. The food
types consisted of grasses, forbs, and dead understory.
Food types from each bag were weighed to determine the
amount of forage within each sampled quadrat, and then
added to obtain total dry matter harvested from all twelve
quadrat squares for each stand.
2.6 Chemical analyses
After separation into food types, a composite food type
sample for each stand was ground in a Wiley Mill with a
1 mm screen, and analyzed for dry matter content [48]
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(Method 930.15), neutral detergent fiber (NDF), acid
detergent fiber (ADF) [49], and crude protein (CP) [48]
(Method 990.03). Total digestible nutrients (TDN) were
calculated from CP and fiber using equations from Weiss
(1992) [50] as an estimate of digestible energy of the
samples [51,52]. The amount of hemicellulose was
determined by subtracting ADF from NDF.
Phenolic glycosides were extracted from 40 mg of freezedried leaf material in 1 ml of methanol. The samples were
vortexed on high for 5 minutes and centrifuged at 16,000
G for 2 minutes. Supernatants were removed and placed
in separate micro-centrifuge tubes. This procedure was
repeated a second time, and the extracts were pooled to
yield 2 ml of crude extract. Phenolic glycosides
(salicortin and tremulacin) were quantified using high
performance liquid chromatography (Agilent 1100 Series,
Santa Clara, CA, USA) with a Luna 2, C18 column (150
x 4.6 mm, 5 μm) at a flow rate of 1 ml/min. Compound
peaks were detected at 280 nm using purified salicortin
and tremulacin standards isolated from aspen leaves [53].
Condensed tannins were extracted from approximately 50
mg of freeze-dried leaf tissue with 1 ml of a 70% acetone10 mM ascorbic acid solution. Samples were vortexed on
high for 20 minutes at 4 °C followed by centrifugation at
16,000 G for 2 minutes. Supernatants were removed and
placed in separate micro-centrifuge tubes, and the
extraction was then repeated. Condensed tannin
concentrations were measured spectrophotometrically
(SpectraMax Plus 384, MDS, Toronto, Canada) using the
acid butanol method [54] standardized with purified
condensed tannins isolated from aspen leaves [55].
Defense content of the understory forage samples was not
assessed given the minimal to nil content of chemical
defenses in grasses and dead plant material and
uncertainties about the type of chemical defenses present
in forbs.
2.7 Statistical analyses
2.7.1 Multivariate analysis–Non-metric multidimensional
scaling (NMDS) ordination
An exploratory ordination of relationships between the
thirteen foodscape variables within each of the fifteen
stands (understory nutritional constituent biomass,
understory food type biomass, aspen defense chemistry
[tremulacin, salicortin, total PG, condensed tannins]) and
aspen browsing indicators (percent browsed aspen, fecal
pellets), indicators of aspen resilience (recruitment stems
ha-1, recruitment TPA, regeneration stems ha-1, live
aspen stems ha -1), stand structure (canopy height,
percent aspen cover), or physiographic conditions
(elevation, slope, aspect) was conducted using nonmetric
multidimensional scaling (NMDS) ordinations to uncover
the variable(s) that explained the most variability between
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foodscapes. Ordinations were created with subsequent
fitting of smooth response surfaces of aspen browsing
indicators, aspen resilience indicators, stand structure
factors, and physiographic conditions over the ordination
to assess the relationship of these groups of variables with
the foodscape.
We used NMDS with Bray-Curtis dissimilarity as
implemented by the metaMDS and ordisurf functions in
the vegan package Version 2.4-1 [56] in R Version 3.3.1
using RStudio [57,58]. Scaling was automatically applied
by the metaMDS command (centering, PC rotation, halfchange scaling). Expanded scores were based on
Wisconsin and square root transformations, as set by
metaMDS. Percent stress, the percentage of variation not
explained by all dimensions in the ordination and
therefore the overall measure of quality of fit of the
ordination to the data, was calculated using the metaMDS
command in the vegan package [59]. The command
envfit with 1,000 permutations was used to obtain r2 and
P-values for all aspen browsing indicators, aspen
resilience indicators, stand structure, and physiographic
variables on each foodscape group ordination.
2.7.2 Univariate correlation analysis
Univariate correlations were conducted after completing
the multivariate analysis to further explore relationships
between the foodscape and indicators of aspen browsing,
aspen resilience, and other biotic and physiographic
conditions assessed. The objective was to obtain one r2
and P-value for each of the individual thirteen foodscape
variables in relation to each of the indicators of aspen
browsing, aspen resilience, stand structure, and
physiographic condition variables because the vegan
package in R only generates one r2 and P-value for each
of these variables in relation to the entire foodscape (not
to the individual variables that make up the foodscape).
Multivariate analyses (i.e., from the NMDS ordination
analyses) with resulting P-values of 0.1 or lower were
included in univariate regressions with foodscape
variables (i.e., food type biomass, nutritional biomass
constituents, and aspen defense chemical constituents).
Those variables included in the univariate analysis were
canopy height and elevation.
We used the xyplot command for regressions using the
lattice package Version 0.20-33 [60] in R Version 3.3.1
using RStudio [57,58]. A significant correlation was
defined as any variable with a P-value of 0.1 or less, and
trends were defined as any variable with a P-value of 0.2
or less.
III.
RESULTS
3.1 Multivariate analysis–Non-metric multidimensional
scaling (NMDS)
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Two convergent solutions were found after 20 runs using
metaMDS analyses for understory food type biomass ha -1,
total understory nutritional constituent biomass ha-1, and
aspen defense chemistry. Two dimensions (k=2) were
selected by the metaMDS function (NMDS stress
value=0.129) and no outliers were removed.
Significant relationships were found between the
foodscape and canopy height as well as between the
foodscape and elevation (see Table 2 for r2 and P-values).
Using our significance criteria, other variables in the
aspen structure and physiographic variable groupings and
variables in the aspen browsing or stand resilience
groupings showed no relationship with the foodscape.
Areas with high forb biomass and low amounts of dead
understory and low condensed tannin concentration in
aspen leaves occurred in stands at high elevation (~2,700
m; see Fig 2) and in stands with high canopy heights (~85
m; see Fig 3). Total nutrient biomass and PG content in
aspen leaves were greatest in stands at intermediate
elevations (~2,525 m) and with intermediate canopy
heights (~67 m).
Table.2: P-values and r2 values from the NMDS
analysis conducted between the foodscape and
indicators of aspen resilience, aspen browsing, and
other biotic and physiographic factors assessed at
the Wolf Creek ranch. Significant relationships are
shown in bold.
r2
P-value
-1
Live aspen stems ha
0.0636
0.6603
Percent aspen cover
0.1376
0.3826
Canopy height
0.5286
0.0099
Elevation
0.6077
0.0019
Aspect
0.0114
0.9380
Slope
0.1940
0.2667
Total pellets ha-1
0.0864
0.5614
TPA recruitment stems 0.0013
0.9940
ha-1
Recruitment stems ha-1 0.0919
0.5714
Regeneration stems ha 0.1549
0.3626
1
Percent browsed aspen
0.0824
0.6093
3.2 Univariate correlation analyses
3.2.1 Canopy height
There was a positive correlation between canopy height
and understory forb biomass ha-1, and a negative
correlation between canopy height and understory shrub
biomass ha-1. We also found a positive correlation
between tremulacin content in aspen leaves and aspen
canopy height, and a positive trend between total PG
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content in aspen leaves and aspen canopy height (see
Table 3 for r2 and P-values).
3.2.2 Elevation
A positive correlation was found between elevation and
both understory grass and forb biomass ha-1, and a
negative correlation between elevation and both
understory dead and shrub biomass ha-1. A positive
correlation was also found between elevation and
understory ADF, NDF, hemicellulose biomass ha-1, and
tremulacin, salicortin, and total PG content in aspen
leaves. Additionally, a positive trend was found between
elevation and understory TDN and CP biomass ha-1 (see
Table 3 for r2 and P-values).
[Vol-2, Issue-2, Mar-Apr, 2018]
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gradient of elevation in each of the fifteen stands (dark
green topographical surface, with each topographical
line labeled with values ranging from 2400 to 2650
meters). The stress value was 12.9%. Stand numbers (1
through 15) appear on the surface in black lettering.
3.3 Nutritional analyses
Crude protein (CP) content was similar between aspen
leaves collected from all fifteen stands, as well as shrub
leaves and forbs collected from the understory of high
recruitment TPA stands (Table 4). In general, CP
concentration was low in grasses and dead plant material
collected from the understory, particularly for high and
medium recruitment TPA locations (P>0.05), and were
lower than CP content of forbs in medium and low
recruitment TPA stands (P<0.05). Acid (ADF) and
neutral (NDF) detergent fiber content was low in aspen
and shrub leaves, with high concentrations in dead plant
material and grasses. Total digestible nutrient (TDN)
concentration was the greatest in aspen and shrub leaves.
Concentration of TDN was lowest in dead plant material
for all recruitment TPA levels, and lowest in grasses for
low recruitment TPA locations (P<0.05).
Fig.2: Organization of the foodscape variables in a
nonmetric multidimensional scaling (NMDS) ordination
showing the first two dimensions.
Foodscape variables were measured in each stand
(fifteen values [stands] for each of the thirteen foodscape
variables). Foodscape variables appear in the ordination
in
maroon
lettering
and
are
as
follows:
-1
grasskgha_biomass (kg of grass ha ), forbkgha_biomass
(kg of forbs ha-1), deadkgha_biomass (kg of dead plant
material ha-1), shrubkgha_biomass (kg of shrubs ha-1),
totalkgha_cp (kg total CP [crude protein] ha -1),
totalkgha_adf (kg total ADF [acid detergent fiber] ha -1),
totalkgha_ndf (kg total NDF [neutral detergent fiber] ha 1
),
totalkgha_hemi (kg total hemicellulose ha -1),
totalkgha_tdn (kg total TDN [total digestible nutrients]
ha-1),
aspen_percenttrem
(percent
tremulacin),
aspen_percentsal (percent salicortin), aspen_percentpg
(percent total PG), and aspen_percenttannin (percent
condensed tannins). Overlaid response surfaces were
placed over the ordination surface representing a
www.aipublications.com
Fig.3: Organization of the foodscape variables in a
nonmetric multidimensional scaling (NMDS) ordination
showing the first two dimensions.
Foodscape variables were measured in each stand
(fifteen values [stands] for each of the thirteen foodscape
variables). Foodscape variables appear in the ordination
in
maroon
lettering
and
are
as
follows:
grasskgha_biomass (kg of grass ha-1), forbkgha_biomass
(kg of forbs ha-1), deadkgha_biomass (kg of dead plant
material ha-1), shrubkgha_biomass (kg of shrubs ha-1),
totalkgha_cp (kg total CP [crude protein] ha-1),
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totalkgha_adf (kg total ADF [acid detergent fiber] ha -1),
totalkgha_ndf (kg total NDF [neutral detergent fiber] ha 1
),
totalkgha_hemi (kg total hemicellulose ha -1),
totalkgha_tdn (kg total TDN [total digestible nutrients]
ha-1),
aspen_percenttrem
(percent
tremulacin),
aspen_percentsal (percent salicortin), aspen_percentpg
(percent total PG), and aspen_percenttannin (percent
condensed tannins). Overlaid response surfaces were
placed over the ordination surface representing a
gradient of canopy height in each of the fifteen stands
(dark green topographical surface, with each
topographical line labeled with values ranging from 40 to
85 meters). The stress value was 12.9%. Stand numbers
(1 through 15) appear on the surface in black lettering.
Table.3: P-values and r2 values from univariate regression
analyses conducted between the foodscape and canopy height
and elevation assessed at the Wolf Creek ranch. Significant
relationships are shown in bold.
Food type biomasse
Grass
Forb
Dead
Shrub
r2 P- r2 P- r2 P- r2
Pva
va
va
val
lu
lu
lu
ue
e
e
e
< 0.
0. 0.
0. 0.
0.
0.0
Canop 0. 97 3
65 47 1
03 0
y
0
2
3
Height 1
f
Elevati
onf
0.
3
1
0.
03
0.
2
0
0.
09
Nutrient constituent biomasse
CPa
ADFb
r2
Canop
y
Height
Elevati
on
0.
0
3
0.
1
6
Pva
lu
e
0.
56
0.
14
r2
0.
0
2
0.
2
4
Pva
lu
e
0.
66
0.
06
Aspen defense chemistryg
Tremul Salicort
acin
in
r2
Pva
r2
Pva
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0.
2
4
0.
06
NDFc
r2
0.
0
1
0.
2
2
Pva
lu
e
0.
69
0.0
1
Hemicell
ulose
r2
Pval
ue
TDNd
0.
01
0.
0
1
0.7
4
0.
06
0.
27
Pva
Condens
ed
Tannin
r2
Pval
Total
PG
r2
0.
39
0.0
5
r2
0.
1
7
Pva
lu
e
0.
70
0.
13
Canop
y
Height
Elevati
on
[Vol-2, Issue-2, Mar-Apr, 2018]
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0.
2
2
0.
4
5
lu
e
0.
08
0.
01
0.
1
0
0.
3
7
lu
e
0.
25
0.
02
0.
1
5
0.
4
3
lu
e
0.
16
ue
0.
05
0.4
4
0.
01
0.
05
0.4
4
a
Crude protein
Acid detergent fiber
c
Neutral detergent fiber
d
Total digestible nutrients
e
Kg ha-1 on a dry matter basis
f
Meters
g
Percent dry matter basis
b
3.4 Plant secondary compound analyses
Total concentration of phenolic glycosides (PG) and
condensed tannins were similar in high, medium, and low
recruitment TPA stands, before and after excluding stands
that did not contain trees between 2 to 2.5 meters in
height (i.e., stand 22 [high recruitment TPA], 16 [medium
recruitment TPA], and 17 [low recruitment TPA]) (see
Table 5).
IV.
DISCUSSION
Previous research suggests that nutrients and plant
secondary compounds (PSC) influence aspen use by
ungulates [5,6,23,61,62]. However, little work has been
completed on the interplay between the chemicals present
in the landscape and aspen stand health and browsing by
ungulates. Here we document relationships of stand
resilience
indicators
(regeneration,
recruitment,
recruitment TPA), aspen browsing indicators (fecal
pellets, percent browsed aspen), structural characteristics
of the stand (canopy height, aspen canopy cover), and
physiographic conditions (elevation) with the foodscape
(understory food type biomass, nutritional constituent
biomass of the understory, and aspen defense chemistry).
4.1 Nutritional constituent biomass
We predicted that as understory nutritional biomass at the
sampled locations increased (e.g., greater crude protein
content, lower fiber content, greater TDN content), aspen
use by ungulates would decline, and consequently
recruitment and regeneration would increase because
ungulates would prefer a higher quality and abundant
understory to less nutritious and defended aspen tissues.
We did not find any significant relationships between
nutritional constituent biomass and aspen use indicator
variables within the ordination, but did find a relationship
between nutritional constituent biomass and elevation.
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The positive relationships found with elevation in the
analyses are likely due to environmental influences such
as precipitation or soil moisture content. Previous studies
have shown elevation is positively correlated with
moisture [63,64]. Locations at higher elevation have
greater soil moisture than those at lower elevations and
aspen, grasses, and forbs tend to thrive in areas of high
moisture versus areas with low moisture [65-67], offering
a greater concentration of nutrients to herbivores. Thus,
the growth and establishment of different food types at
various elevations on the landscape affected the quality of
the foodscape (e.g., food type biomass and therefore
nutrient amount and concentration), essentially providing
a resilience buffer not present at lower elevations.
Table.4: Nutritional analyses (% dry matter) of aspen
leaves and understory samples collected from different
aspen stands at Wolf Creek Ranch showing different
levels of aspen recruitment TPA.
High recruitment TPA aspen stands- # 1b, 9 a, 11e, 13e,
15d
Crude
ADFf
NDFg
TDN
h
protein
Grasse 11.5 ± 2.1
38.11 ±
61.89 ±
56.17
s
1.39
1.72
±
1.82
Forbs 13.71±1.4
30.9±1.42
42.56±2.5
59.22
5
±
1.16
Dead
11.11±0.5
44.64±1.0
64.71±1.0
51.01
4
1
4
±
0.73
Aspen 14.73±0.3
18.39±1.5
26.26±1.6
69.12
1
2
5
±
1.08
Medium recruitment TPA aspen stands- # 3d, 4a, 6d, 8e,
14c
Crude
ADF
NDF
TDN
protein
Grasse 8.89 ±
40.05 ±
65.76 ±
53.74
s
0.48
0.57
1.54
±
0.56
Forbs 11.87±1.3
32.68±3.9
42.57±3.2
57.76
3
1
±
3.12
Dead
8.88±0.59
45.53±0.9
65.32±2.5
49.52
1
4
±
0.75
Aspen 14.53±0.8
17.43±0.5
24.96±2.2
69.86
8
3
±
0.39
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Low recruitment TPA aspen stands- # 2b, 5d, 7c, 10c, 12c
Crude
ADF
NDF
TDN
protein
Grasse 8.97 ±
40.78 ±
66.03 ±
53.21
s
0.08
0.72
0.29
±
0.58
Forbs 12.26±0.4
30.33±2.9
42.21±2.9
59.62
1
4
9
±
2.30
Dead
11.56±0.2
41.76±0.6
61.57±1.3
53.38
1
1
7
±
0.46
Aspen 14.84±0.5
20.29±1.1
29.21±1.4
67.62
8
9
9
±
0.85
Composite leaf samples from all stands sampled
Crude
ADF
NDF
protein
Shrub 13.24
17.71
27.80
TDN
69.60
a
August 25, 2015
August 26, 2015
c
August 27, 2015
d
August 28, 2015
e
August 29, 2015
f
Acid detergent fiber
g
Neutral detergent fiber
h
Total digestible nutrients
b
Table.5: Plant secondary compounds (% dry matter) of
aspen leaves at Wolf Creek Ranch across stands with
different levels of recruitment TPA.
High recruitment TPA aspen stands
Tremulacinf Salicortinf Total Condensed
PGf
tannins
g
Aspen 5.13 ± 0.99 8.33 ±
13.47 1.59 ±0.56
1.81
±
2.71
Aspenh 5.04 ± 0.75 7.73 ±
12.77 2.42 ± 2.04
1.52
±
2.18
Medium recruitment TPA aspen stands
Tremulacin Salicortin Total
PG
Aspeng 6.15 ± 1.72 8.55 ±
14.7
2.95
±
4.62
Aspenh 6.33 ± 1.3
9.08 ±
15.41
2.29
±
3.55
Condensed
tannins
1.68 ± 0.92
1.55 ± 1.41
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Low recruitment TPA aspen stands
Tremulacin Salicortin
Aspeng
Aspenh
6.04 ± 0.9
5.59 ± 0.84
6.05 ±
1.38
5.5 ± 1.2
Total
PG
12.09
±
2.03
11.09
±
1.89
Condensed
tannins
2.97 ± 1.16
2.66 ± 1.87
a
August 25, 2015
August 26, 2015
c
August 27, 2015
d
August 28, 2015
e
August 29, 2015
f
Percent of dry sample weight
g
Excluding stands that did not contain 2 m trees for
sampling
h
Including stands that did not contain 2 m trees for
sampling
b
4.2 Understory food type biomass
We also predicted that understory biomass would be
inversely related to aspen browsing because if nutrient
biomass at these locations was above the threshold
required to meet nutritional needs, then animals did not
need to seek extra nutrients from aspen leaves and
consequently aspen use would decline. We found a
significant effect of elevation on understory biomass, and
as mentioned in the previous section, elevation is
positively correlated with moisture [63,64]. Aspen and
forbs tend to thrive in areas of high moisture (high
elevations) [65-67], and grasses and forbs senesce when
temperatures increase and less moisture is available to the
plants. Shrubs establish in warm and dry climates [65],
and therefore thrive at lower elevations. These patterns
are in agreement with findings from the univariate
analysis in the current study, with positive associations
between elevation and understory forb and grass biomass,
with negative correlations between elevation and shrub
biomass. Differences in forage types across elevations
may influence elk foraging distribution, as well as aspen
recruitment and regeneration. For instance, elk may use
more aspen at locations where understories offer lower
biomass (e.g., shrubs at lower elevation), a selection
process with negative impacts on aspen recruitment and
regeneration. Nevertheless, our results do not provide an
indication of this pattern, likely due to the influence of
other intervening variables in a complex landscape, which
were more consequential than the differences in biomass
and chemistry observed across the gradient explored in
this study. For instance, it is possible that locations at
higher elevation, due to water availability, may be simply
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[Vol-2, Issue-2, Mar-Apr, 2018]
ISSN: 2456-8791
more resilient–i.e., able to replace browsed stems at a
high enough rate to not experience growth limitation
through compensatory growth.
4.3 Defense content in aspen
Lastly, we predicted that as defense content in aspen
stands increased, aspen use would decrease because
phytochemicals constrain intake. As with nutrient
constituent biomass and food type biomass, aspen use
indicators did not show any relationship with the
foodscape but elevation and canopy height did. Although
no straightforward explanations for the relationship
between aspen defense content and canopy height or
elevation emerged from the current study, possible
explanations may be found in current understandings of
the relationship between canopy height or elevation and
soil microclimate or total available moisture. As canopy
height increases, the amount of light that reaches the
understory is reduced [68]. Understory light environments
affect microclimate (e.g., solar radiation, soil and leaf
temperature, soil moisture) [69,70], and increased light
intensity can increase soil temperature and soil
evaporation rates [70], which can influence plant
establishment and growth [71,72,73]. Alternatively, the
relationship between canopy height and soil moisture may
be due to bottom-up effects instead of top-down effects—
meaning that soil microclimate may drive canopy height
differences instead of canopy height driving soil
microclimate differences—or soil moisture gradients may
instead be due to elevational moisture influences. Because
we did not measure soil microclimates or determine the
individual effects of canopy height or elevation on PSC
content in aspen, we cannot conclude in which direction
the effect occurs. In either case, increased light intensity
(possibly from changes in canopy height) and temperature
(possibly from changes in canopy height and/or elevation)
has been shown to increase defense chemical content
within aspen stands [27,74-76], but our findings suggest
the opposite–showing increased canopy height (shading)
coincided with increased aspen PG content in the sampled
juvenile aspen trees. Such changes may be in response to
other variables that affect PG content such as
temperature, soil moisture, or soil nutrients that were not
assessed in the current study [27,76].
V.
CONCLUSION
Results from this study show that the foodscape is
influenced by elevation and canopy height, but no
relationships were found with indicators of aspen
herbivory or stand condition. The abundance of forbs and
grasses at higher elevation locations helped to explain the
distribution of CP biomass across the foodscape. In
contrast, stands with low CP and TDN concentrations in
the understory were found at lower elevation locations. It
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is likely that foodscapes with more differences than those
found in the present study may help explain greater aspen
herbivory and less aspen regeneration and recruitment at
low-quality locations (i.e., even lower levels of CP or
TDN biomass) relative to those that offer more food
alternatives with lower concentrations of plant defenses
and greater nutritional quality. Moreover, aspen stands at
lower elevations may be more at risk of succumbing to
overbrowsing because aspen in those areas are more
likely to be stressed from lack of moisture [66,67,77].
The concept of foodscape and foraging by ungulates
developed in this study could be used to explore other
relationships, on a wider range of landscapes–like
browsing and mineral content of aspen trees and
understories–to address concerns of overbrowsing in
aspen-dominated communities.
VI.
CONFLICTS OF INTEREST
The authors declare that they have no conflict of interest.
VII.
STATEMENT OF HUMAN AND ANIMAL
RIGHTS
This article does not contain any studies with human
participants or animals performed by any of the authors.
VIII. ACKNOWLEDGEMENTS
We would like to thank Jim and Katie Schuler all their
help, for opening their property and yurt to us, and
allowing us to conduct sampling and analyses, and for the
coauthors on the original publication: Allison Jones and
James Catlin with the Wild Utah Project, Arthur Morris
with the Utah Open Lands Conservation Association, and
Michael Kuhns with USU Wildland Resources
Department and Forestry Extension. We would also like
to thank Susan Durham with the USU Ecology Center
and Peter Adler with the USU Wildland Resources
Department for their assistance with development of
statistical analyses. This paper is published with the
approval of the Director, Utah Agricultural Experiment
Station, and Utah State University, as journal paper
number 9010.
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