Shrub-Grass Interactions in Relation to
Cattle Grazing in Atriplex canescens
Andrés F. Cibils
Richard H. Hart
David M. Swift
Abstract—Two related studies conducted at a shrub-dominant site
on the shortgrass steppe in Colorado showed that: (a) relative
numbers of young fourwing saltbush (Atriplex canescens [Pursh]
Nutt.) shrubs decreased significantly with increasing aboveground
biomass of western wheatgrass (Pascopyron smithii Rydb); (b) there
were significant seasonal variations in the levels of cattle utilization
of young shrubs; and (c) utilization of young shrubs was significantly associated with increases in the proportion of C4 grasses in
cattle diets. Herbaceous understory at this site may affect shrub
population dynamics both directly, through shrub-seedling/grass
competition in the absence of grazing, and indirectly, by influencing
cattle foraging behavior.
Fourwing saltbush grows in relatively dense stands on
creek floodplains and terraces of the shortgrass steppe in
northeastern Colorado. Edaphic factors appear to control
the occurrence and distribution of shrub-dominant communities in this grassland ecosystem (Lauenroth and Milchunas
1991). Biotic processes such as grazing can affect shrubgrass interactions and exert a strong influence on the relative abundance of grasses and woody plants at a given point
in time (Archer 1995 and references therein). At our research site, western wheatgrass dominates the shrub
interspaces in ungrazed exclosures. Interactions between
cattle grazing regime and adult fourwing saltbush size and
density are thought to create the necessary conditions for
western wheatgrass proliferation (Hart and others 1997). As
opposed to what occurs with this rhizomatous grass, numbers of juvenile fourwing saltbush shrubs in exclosures are
extremely low relative to surrounding grazed pastures (Cibils
and others 1997). We examined the relation between biomass of western wheatgrass in the shrub understory and
proportion of young shrubs to determine whether these
variables were significantly associated.
Fourwing saltbush is fairly sensitive to defoliation (Buwai
and Trlica 1977; Trlica and others 1997). Adequate periods
of rest are required to maintain viable shrub populations
under grazing (Pieper and Donart 1978; Price and others
In: McArthur, E. Durant; Ostler, W. Kent; Wambolt, Carl L., comps. 1999.
Proceedings: shrubland ecotones; 1998 August 12–14; Ephraim, UT. Proc.
RMRS-P-11. Ogden, UT: U.S. Department of Agriculture, Forest Service,
Rocky Mountain Research Station.
Andrés F. Cibils is a PhD candidate in the department of Rangeland
Ecosystem Science at Colorado State University, Fort Collins, CO 80523.
Richard H. Hart is a Senior Range Scientist at the High Plains Grasslands
Research Station of the USDA-ARS, Cheyenne, WY 82009. David M. Swift is
an Associate Professor in the Rangeland Ecosystem Science Department and
Senior Scientist at the Natural Resource Ecology Laboratory, both at Colorado State University, Fort Collins, CO 80523.
186
1989). At our research site, cattle grazing (winter grazing in
particular) can have a negative impact on shrub longevity
(Cibils and others, submitted), and can apparently cause
population turnover rates to be higher in grazed stands than
in exclosures (Cibils and others 1997). Consequently, young
shrubs account for up to 35% of the population in grazed
shrub stands at our site (Cibils and others 1997). Young
fourwing saltbush shrubs in seeded stands can be severely
damaged by rabbit, grasshopper, and deer herbivory (Springfield 1970). Little is known, however, about the impact of
cattle grazing on juvenile fourwing saltbush shrubs in natural populations and the factors that control it. At our research site we found that the proportion of young shrubs was
greater in winter-grazed stands than in stands that had
been historically grazed in summer (Cibils and others 1997).
We hypothesized that the impact of moderate and heavy
cattle grazing on juvenile shrubs would be greater in summer than in winter. Since young shrubs are intermingled
with the herbaceous understory, we also hypothesized that
the utilization pattern would be related to the seasonal
dynamics of this layer of the plant community.
Saltbushes (Atriplex sp.) are fairly short-lived shrubs
(Stewart and others 1940; Crisp 1978; Norton 1978; West
1979). Recruitment in many saltbush species is a somewhat
continuous process (Eldridge and Westoby 1991), as opposed
to other dryland shrubs that exhibit episodic recruitment
events (Paur 1971). At our research site, recruitment occurs
almost entirely through sexual reproduction. Hence, factors
that affect seed germination, seedling establishment, and
juvenile shrub survival are crucial to the long-term viability
of these populations.
We conducted our research in a fairly homogeneous
fourwing saltbush stand at a site on the shortgrass steppe in
Colorado. We addressed the following research questions:
(a) is the relative abundance of young shrubs related to the
abundance of western wheatgrass in the shrub interspaces?
(b) are there seasonal and stocking-density-related variations
in the level of cattle utilization of young shrubs? and (c) are
seasonal variations in cattle utilization of young shrubs
related to the dynamics of the herbaceous understory?
Materials and Methods ___________
Our study site was located on a floodplain area close to
Owl Creek, within the USDA-ARS Central Plains Experimental Range (40° 49' N 107° 47' W). Soils of this site have
been described as loamy to sandy loams. Fourwing saltbush,
blue grama (Bouteloua gracilis [H.B.K.] Lag. ex Steud), and
western wheatgrass are the dominant plant species at the
USDA Forest Service Proceedings RMRS-P-11. 1999
USDA Forest Service Proceedings RMRS-P-11. 1999
stocking density, and year were considered fixed effects,
while block was considered a random effect. We included all
possible two-way and three-way interactions between fixed
effects in the final model. We also explored interactions
between fixed and random main effects, and included significant interactions in the final model. Utilization data
were arcsin-transformed in order to meet the assumption of
homogeneity of variances of the ANOVA. The overall level of
significance was set at p = 0.05.
The last research question was addressed by performing
regression analysis between percent C4 grasses in cattle
diets and utilization of marked leaders on young shrubs. In
order to do this we collected fecal material samples (in the
1997 experiments) immediately after removing cattle from
the pastures. These samples were used to determine diet
composition applying microhystological analysis techniques
described by Sparks and Malecheck (1968).
Results ________________________
Biomass of western wheatgrass in the shrub interspaces
explained 80% of the variation in relative numbers of young
shrubs (p = 0.016). Overall, increases in biomass of western
wheatgrass were associated with a significant decrease in
the relative abundance of young shrubs (fig. 1).
Utilization of young shrubs increased significantly as the
growing season progressed and was significantly higher
under heavy stocking densities than under moderate ones
(fig. 2.a,b). Utilization was lowest in January, intermediate
in April, and highest in September, and was always higher
in the high stocking density pastures. This pattern was
consistent across years (table 1). In 1998 overall utilization
of young shrubs was higher than in 1997. A milder winter in
40
Percent young shrubs
site (Liang and others 1989). Mean annual precipitation is
320 mm, most of which occurs between April and September.
The first research question (stated above) was addressed
by revisiting data we had collected in a transect study at our
site in the fall of 1995 that we describe elsewhere (Hart and
others 1997; Cibils and others 1997). We performed linear
regression analysis between percent young shrubs (dependent variable) and aboveground biomass of western wheatgrass in the shrub interspaces (independent variable). We
calculated percent young shrubs and mean western wheatgrass biomass for each of six transects: two in historically
winter-grazed pastures; two in historically summer-grazed
pastures; and two in exclosures.
The second research question was addressed by measuring utilization of marked young shrubs in 12 half-hectare
experimental pastures. The pastures were built in two
parallel blocks of seven adjacent units each (one plot was left
as an exclosure in each block) in the general area where we
had previously placed the transects. We conducted a 2-year
(1997 and 1998) browsing experiment that consisted of
browsing four pastures with cattle for a period of 4 days in
winter (January), early spring (April), and late summer
(September). Two pastures were browsed moderately
(4 heifers) and two were browsed heavily (12 heifers). Moderate stocking densities simulated levels of cattle herbivory
historically imposed on fourwing saltbush stands at the
CPER. High stocking densities were three times the historical (moderate) densities. Cattle used in the experiments
were always taken from herds grazing pastures with abundant fourwing saltbush, so as to minimize dietary and social
adjustment times. We used heifers in all experiments, except for September 1997, when heifers were not available,
obliging us to use steers instead. The mean live weights of
the heifers or steers used ranged from about 400 to 520 kg.
Pastures were assigned randomly to each stocking density
treatment. Randomization was performed within each block
of experimental pastures, subject to the constraint that no
two adjacent pastures were grazed on the same date.
Twenty young shrubs were randomly selected and labeled
in each half-hectare grazing plot. Shrubs were labeled in a
manner that would be inconspicuous to cattle. Small (not
taller than 25 cm) non-reproductive individuals were classified as juvenile shrubs. In the weeks prior to each experiment, four primary leaders were marked on each labeled
shrub. Length of marked leaders was measured prior to
introducing the cattle. Once each experiment was over (and
the cattle removed), length of marked leaders were remeasured. Leaders marked on young shrubs were mono
axial stems seldom exhibiting branches and never exhibiting flowers or fruits. We, therefore, assumed a linear length/
weight relation for such leaders, where percent length removed was assumed to be roughly equal to percent biomass
consumed by cattle.
Mean percent utilization of marked leaders on young
shrubs was calculated for each experimental plot. Data were
analyzed using repeated measures analysis of variance
(ANOVAR). The statistical model selected for the analysis
was a mixed effects repeated measures factorial experiment
design. Season (January, April, and September), stocking
density (moderate and heavy), year (1997 and 1998), and
block (1 or 2) were the factors studied. Season, stocking
density, and block were repeated within year. Season,
30
R 2 = 0.80
p = 0.016
20
10
0
0
100
200
300
400
Western wheatgrass
Biomass (g/m2)
Figure 1—Relationship between aboveground
biomass of western wheatgrass and percent
young shrubs.
187
Utilization of marked leaders
1998 relative to 1997, and less rainfall in the month of July
1998 relative to July 1997 may have contributed to the
significant year effect.
Under moderate stocking density, increases in the content
of C4 grasses in cattle diets were significantly associated
with an increase in utilization of young shrubs (p = 0.011
[fig. 3.a]). Percent C4 grasses in cattle diets explained 83%
of the variation in utilization of young shrubs. Under high
stocking density the relationship between these variables
was somewhat weaker (R2 = 0.63) and marginally significant (p = 0.058) (fig.3.b).
Discussion _____________________
Percent utilization young shrubs
Utilization of marked leaders
The negative association between aboveground biomass
of western wheatgrass and proportion of young fourwing
saltbush shrubs (in relation to the cattle grazing regime) is
consistent with predictions of a conceptual model proposed
by Archer (1995). According to this model, probability of
seedling establishment tends to increase as graminoid shoot
Figure 2—(a) Utilization of marked leaders in high
stocking density (full bars) and moderate stocking
density (empty bars) pastures. (b) Experiment means
for utilization of marked leaders in January, April, and
September.
Fixed effects:
Year
Stocking density
Season
Year*Stocking density
Year*Season
Stocking density*Season
Stocking density*Year*Season
Random effect:
Block
188
df
1
1
2
1
2
2
2
F
72.17
35.24
12.41
0.57
2.48
0.99
0.57
p
<0.001
<0.001
0.002
0.466
0.129
0.403
0.466
Percent utilization young shrubs
Percent C4 grasses in the diet
Table 1—Anova table for arcsin transformed percent utilization of
marked leaders on young shrubs.
Source
R 2 = 0.83
p = 0.011
R 2 = 0.63
p = 0.058
Percent C4 grasses in the diet
1
0.0007
0.980
Figure 3—Relationship between percent C4 grasses
in cattle diets and utilization of marked leaders on
young shrubs under: (a) moderate stoking density
and (b) high stocking density.
USDA Forest Service Proceedings RMRS-P-11. 1999
and root biomass decreases. Increases in grazing pressure
over time are predicted to favor a decrease in graminoid
biomass and allow seedlings of woody plants to establish.
Archer (1995) stated that grazing can promote shrubseedling establishment by releasing water resources otherwise used by grasses. Situations such as those predicted by
Archer’s (1995) model, where grazing is thought to mediate
shrub-seedling establishment, occur in other species of the
genus Atriplex such as shadscale (Atriplex confertifolia)
(Chambers and Norton 1993).
Seed germination and seedling establishment require
adequate windows of opportunity, which are affected by
climate and other species in the plant community (Booth and
Haferkamp 1995). In fourwing saltbush such “windows” are
apparently related to the simultaneous occurrence of cool
temperatures (around 25 °C) and the availability of sufficient water to allow seed imbibition (Springfield 1970).
Temperatures either above or below 25-28 °C depress germination (Springfield 1970). Utricle bracts of fourwing saltbush can have considerable amounts of saponins (Nord and
Van Atta 1960) that can act as germination inhibitors.
Therefore, water is required not only for imbibition but also
to eliminate water-soluble inhibitors prior to the onset of
enzymatic processes leading to seed germination. Optimal
growth temperatures for C3 grasses are within the range of
20-25 °C (Larcher 1980). On the other hand, C4 grasses grow
optimally at temperatures ranging from 32-40 °C (Larcher
1980). Hence, onset of growth in western wheatgrass (using
available water resources) overlaps considerably with the
narrow window of opportunity for fourwing saltbush seed
germination. Conversely, by the time active growth of blue
gramma (dominant in the understory of grazed stands)
occurs, temperatures are far from optimal for fourwing
saltbush seed germination. The taller canopy structure of
western wheatgrass (relative to blue gramma) favors the
interception of larger amounts of rainwater and light, thus,
decreasing still more the probabilities of successful shrub
seed germination and/or seedling survival. Hence, while the
grass/young-shrub relation we measured does not necessarily imply a cause-effect relation, there are a number of
physiologically-based explanations that suggest that the
statistical association we found is biologically meaningful.
Utilization of juvenile shrubs was highest in summer,
intermediate in spring, and lowest in winter, and always
higher under high stocking densities than under moderate
ones. Seasonal patterns of utilization of juvenile shrubs
were the same in both years, and persisted under a threefold increase in stocking density. Heavy defoliation can
promote mortality of adult fourwing saltbush shrubs (Buwai
and Trlica 1977; Trlica and others 1977; Pieper and Donart
1978). Atriplex canescens is more sensitive to heavy defoliation than other species of its genus (Benjamin and others
1995). Fourwing saltbush seedlings can also be affected
negatively by herbivory. Survival in seedling plots exposed
to grasshopper, rabbit, and deer herbivory was only 67% of
protected controls (Springfield 1970). While little is known
about how cattle grazing affects juvenile fourwing saltbush
shrubs, studies conducted with other shrub species suggest
that livestock may increase natural mortality rates of young
shrubs. Cattle grazing promoted grater mortality of juvenile
basin big sagebrush shrubs (Artemisia tridentata Nutt ssp.
USDA Forest Service Proceedings RMRS-P-11. 1999
tridentata Beetle) compared to adults of the same species
(Owens and Norton 1990). In another set of experiments, big
sagebrush seedlings exhibited higher mortality rates in
shrub interspaces grazed by either sheep or cattle relative to
ungrazed exclosures (Owens and Norton 1992). Revegetated
rangelands grazed by horses and deer suffered greater
mortalities of big sagebrush juveniles relative to the ungrazed
controls (Austin and others 1994). Assuming that shrub
mortality increases with increasing levels of herbivory (as
suggested in the literature), survival of juvenile fourwing
saltbush shrubs at our site would be expected to be lowest
under summer grazing, intermediate under spring grazing
and highest under winter grazing by cattle.
Utilization levels of juvenile fourwing saltbush shrubs at
our site increased significantly with increasing proportion of
warm season grasses in cattle diets both in moderately and
heavily stocked pastures. Cattle are generally roughage
eaters (Hofmann 1989), and can feed more efficiently on the
herbaceous understory than on shrubs (Petersen and others
1994). Anatomical adaptations that enable cattle to harvest
large volumes of forage on a daily basis constrain their
ability to be selective feeders (Van Soest 1994). On the
shortgrass steppe cattle shift from a shrub-grass diet in
winter to a grass-dominant diet in spring and summer
(Schwartz and Ellis 1981; Shoop and others 1985). When
high quality herbaceous forage is available in adequate
amounts, cattle apparently feed predominantly on grasses
and forbs in the herbaceous understory (Cibils, unpublished
data). It is therefore not surprising that juvenile fourwing
saltbush shrubs in our experiments (intermingled in the
herbaceous canopy) were utilized the most at times of the
year when cattle were feeding primarily on grasses. This
implies that seasonal increases in utilization of juvenile
shrubs at our site were a consequence of the phenology of the
herbaceous understory, rather than of the direct dietary
selective behavior of cattle. Young shrubs were possibly
most heavily utilized in summer because cattle could not
help harvesting them together with the bulk of herbaceous
forage they were feeding on.
Grasses may have an important influence on population
dynamics of fourwing saltbush at our site. In the absence of
grazing, asymmetric competition interactions between
grasses and shrub seeds or seedlings may result in reduced
(or no) shrub recruitment. In stands grazed by cattle, grasses
may indirectly affect survival of juvenile individuals by
influencing cattle foraging behavior.
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