Predisposition of Willows to Elk Browsing
Due to Willow Interactions with Abiotic
Factors
Rex G. Cates
Jiping Zou
Stuart C. Wooley
Francis J. Singer
Lauryl C. Mack
Linda Zeigenfuss
Abstract—Current literature indicates that the decrease in willow
stature and productivity on the winter range in Yellowstone National Park is due to a complex interaction among abiotic and biotic
factors. Lack of change in soluble carbohydrates, total phenolics and
tannins when willows were mechanically clipped in exclosures in
Yellowstone National Park show that willows were not able to
respond physiologically to these treatments. These data are supportive of the premise that the willow decline is due to unfavorable
growing conditions on the northern winter range. Willow physiology, growth, and recruitment are impacted adversely by ungulate
browsing, but experimental manipulations within exclosures indicate that browsing may not be the only important factor. The trend
toward aridity, lowered water tables, reduced stream flow, lack of
flooding, and absence of beaver are suggested to be important
factors in reduced willow production, reproduction, and lower levels
of primary and defensive chemicals.
Over the last 60 years large decreases in willow (Salix
spp.) populations and stature have occurred in the northern
winter range in Yellowstone National Park (YNP), Wyoming
(Wagner and others 1995a; Chadde and Kay 1991; Houston
1982). Willow declines have been especially dramatic occurring primarily between 1920 and 1940 during an extended
drought (Engstrom and others 1991). Reasons for these
changes in willow dyamics have been heavily debated resulting in several hypotheses. The most common is that elk
(Cervus elaphus) have increased to unnaturally high levels
due to reduced predation including hunting, alterations of
the landscape by modern man, and disruption of migration
routes (Wagner and others 1995b; Boyce 1991; Pengally 1963).
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.
Rex G. Cates and Jiping Zou are the Director and Associate Director,
respectively, of the Chemical Ecology Laboratory, and Stuart C. Wooley,
Research Assistant, Department of Botany, Brigham Young University,
Provo, UT 84602. Francis J. Singer and Linda Zeigenfuss, Research Ecologist
and Ecologist, respectively, Biological Division of the U.S. Geological Survey,
Midcontinent Ecological Center, Natural Resources Ecology Lab, Colorado
State University, Fort Collins, CO 80523. Lauryl C. Mack is a Wildlife
Biologist, P.O. Box 168, Yellowstone National Park, WY 82190.
USDA Forest Service Proceedings RMRS-P-11. 1999
A second set of hypotheses focus on climate and hydrological changes in conjunction with beaver declines. For the
winter range in Yellowstone National Park climates are
warmer and drier this century (Balling and others 1992a,b),
which is suggested to have resulted in lower water tables as
judged by stream downcuts, reduced stream flows, and less
flooding. These changes may foster a habitat that is unfavorable for willow growth and recruitment (Singer and others
1994; Houston 1982). Compounding these adverse effects on
willows is the decline in beaver, which has resulted in almost
no beaver ponds, a change in stream flows, and lower water
tables (Jonas 1955). Most likely, with fewer beaver ponds
reestablishment sites for willow shoots, sprouts, and seedlings are greatly diminished and nutrient dynamics may
have changed significantly (Naiman and others 1986; Naiman
and Melillo 1984). Changes in these climatic and hydrological factors combined with the loss of beaver are purported to
have resulted in willows that are unable to produce sufficient natural defenses against ungulates. As a result, willows become nutritionally more suitable to these large herbivores and are not able to grow beyond the height of
browsing.
Although heavy browsing exacerbates willow physiology
and growth, we suggest that elk browsing may not be the
only cause of willow declines. We posit that changes in water
dynamics due to reduced precipitation, higher temperatures, reduced flooding, lowered water tables, and the absence of beaver may be important factors causing the demise
of willows on the northern winter range. In support of the
climate-hydrological-beaver scenario, tall productive willows growing within the upper reaches of the drainages
where the habitat is more favorable for growth were browsed
seven to nine times more than were suppressed willows at
lower elevations (Singer and Cates 1995).
Willow Chemistry and Ungulate Browsing
Compounds in willows that function as defenses against
herbivores and also affect nutritional quality are tannins
that bind to several primary metabolites (e.g., nitrogencontaining compounds like proteins, amino acids, DNA,
RNAs), and low molecular weight phenolics, which are
suggested to be toxic and/or act as feeding deterrents (Robbins
1993). Of these two, low molecular weight phenolics may
191
play the major role in deterring ungulate browsing since
some large animal browsers may render tannins less effective as defenses (Robbins and others 1987). For willows
inhabiting sites favorable for growth, the challenge from
tissue removal by herbivores and infection from pathogens
normally results in an induced increase in phenolics and
tannins in remaining and new leaf and stem tissues (Karban
and Baldwin 1997). Where conditions for willow growth are
unfavorable on the northern winter range, willows will not
be able to respond by increasing their production of defensive chemicals when exposed to heavy ungulate browsing
and mechanical clipping experiments.
Clipping experiments using willows have produced mixed
results regarding changes in nitrogen and soluble carbohydrates in new growth. Clipping Bebb willow (S. bebbiana)
resulted in no significant increase in carbohydrates, total
nitrogen, and phosphorus (Chapin and others 1985), but
clipping S. lanata at 0, 50, and 100% for 2 years resulted in
a significant increase in total nitrogen and phosphorus
(Ouellet and others 1994). In this same study soluble carbohydrates decreased significantly and then returned to control levels. An important contribution of the study reported
here is the determination of carbohydrate concentrations
over a 3 year period in which willows located inside exclosures were clipped at 0, 50, and 100% of their current annual
growth.
Objectives and Hypotheses _______
Our objectives were first to test hypotheses, in the context
of the climate-hydrological-beaver paradigm, regarding the
physiological status of willows on the northern winter range
of Yellowstone National Park. Secondly, we summarize
from the literature the characteristics purported or documented for sites deemed to be unfavorable or favorable to
willow growth, productivity, and recruitment, and a description of willow responses to these site characteristics. Included in this summary are projections as to how ecosystem
processes may change as site conditions change, and the
communities that result from alteration of these processes
(Naiman and others 1988; Cummins and others 1989). The
hypothesis tested is that willows from which the current
annual growth (CAG) was mechanically clipped at the 50
and 100% levels inside exclosures in YNP will not be able to
respond, as compared to the control (0% clip), by increasing
defensive phenolic and tannin compounds. The response in
carbohydrates to these treatments is mixed, but the expectation is that total soluble carbohydrate content will decrease in the presence of mechanical clipping as compared to
the control. Clipping experiments inside 30-35 year old
exclosures should be particularly instructive since the effect
of elk browsing is eliminated, and the experiments were
carried out over a 3-year period.
Study Areas and Methods ________
Study Sites
Study areas, and the indepth analysis of climate, growth,
and physiological data, are detailed in Singer and others
(1998). In summary, the northern winter range in YNP is
192
about 140,000 hectares located on the northern boundary of
the park. This area is characterized by cold winters (averaging –4.90°C) and short, cool summers (15°C) with mean
annual precipitation averaging about 18-40cm/year
(Houston 1982). At the time of this study, elk population
2
densities on the YNP winter range were 11-16 elk/km .
Beaver, however, are rare or absent on the winter range in
YNP (<1% of stream length with beaver activity).
Primary and Secondary Metabolites
Ten to 15 shoots from each plant were analyzed for total
soluble carbohydrates, phenolics, and tannins, and were
expressed on a dry-weight basis. ANOVA for unequal sample
sizes on log transformed data were performed using clipping
treatment as the independent variable, and total content of
soluble carbohydrates, phenolics, and tannins as the dependent variables.
Results and Discussion __________
Willow Physiology as an Indirect
Indication of Unfavorable Habitat Quality
for Willow Growth
Measurements of primary and secondary metabolites
over a 3 year period indicate that 50 and 100% clipped
willows in exclosures in YNP were not able to respond to
these treatments by increasing phenolic and tannin content
(tables 1,2). Soluble carbohydrates for Bebb willow and false
mountain willow (S. pseudomonticola) did not change or
decrease significantly in the 50 and 100% treatments (e.g.,
false mountain, 1996) (tables 1, 2).
Total phenolic content in Bebb (table 1) and false mountain willows (table 2) followed the pattern of not changing
significantly across treatments within a year, or of decreasing significantly (e.g., Bebb willow summer 1993—100%
decreased compared to 50%; for the winter 1995 collection,
50 and 100% decreased compared to 0%). Bebb willow tannin
content in leaf and twig tissues for the 0 and 50% clipped
plants was not significantly different, but tannin content
decreased significantly in the 100% clipped plants compared
to the other two treatments for 1993 (table 1). For the 1995
winter twig collection, tannin content decreased in the 100%
clip compared to the 0 and 50% treatments (table 1). For
false mountain willow the 1993 and 1996 tannin content in
leaf and twig tissues in the summer was not different among
any treatments, but did significantly increase in the 100%
clip in 1995 (table 2). In the 1993 winter collections tannin
content significantly decreased in the 50% treatment compared to the control and 100% clip (table 2).
These physiological data are consistent with the hypothesis that willows in exclosures that have been protected from
browsing 31-35 years were occupying unfavorable habitats
for growth. An additional clue to the willow decline, as
related to water dynamics and improved habitat quality for
willow growth and physiology, is found in the phenolic data
in the clipping experiments. A trend toward increased moisture and lower temperatures in YNP seems to have occurred
during the late 1990’s (Stohlgren and others 1998). This
USDA Forest Service Proceedings RMRS-P-11. 1999
Table 1—Effect of mechanical clipping on total phenolic, tannin, and total soluble carbohydrate content of the current year’s growth of Bebb willow
from July 1993 through summer 1996 ( x , sd§), Yellowstone National Park, Wyoming.
0
Year/compound+
50
Summer
100
Summer
Winter
Winter
1993
Total phenolics
Tannins
Sol. carbo.¤
4380 ± 1226
76 ± 12a*
44 ± 16
5091 ± 1784
57 ± 17
23 ± 1
5191 ± 1357a*
72 ± 8a*
47 ± 12
4349 ± 427
52 ± 7
22 ± 2
3634 ± 1200b*
56 ± 13b*
47 ± 13
5200 ± 1184
55 ± 8
21 ± 8
1995
Total phenolics
Tannins
Sol. carbo.
3071 ± 466
66 ± 8
32 ± 5
6987 ± 1688a*
52 ± 12a*
19 ± 6
3133 ± 688
57 ± 14
29 ± 4
3287 ± 1546b*
53 ± 14a*
20 ± 5
3066 ± 749
57 ± 13
32 ± 14
3873 ± 2246b*
30 ± 10b*
17 ± 1
1996
Total phenolics
Tannins
Sol. carbo.
9154 ± 1595
62 ± 8
26 ± 5
—
—
—
9181 ± 2295
64 ± 7
32 ± 8
—
—
—
Summer
Winter
8953 ± 2950
59 ± 17
28 ± 5
—
—
—
§
Means followed by different letters significantly different at *p ≤0.05; **p ≤0.10, ANOVA.
Total phenolics expressed as average peak height divided by 100. Tannins and soluble carbohydrates expressed as mg/g dry weight.
¤
From S. C. Wooley, M.S. Thesis 1998. Brigham Young University, Provo, UT
+
Table 2—Effect of mechanical clipping on total phenolic, tannin, and total soluble carbohydrate content of the current year’s growth of false mountain
willow from July 1993 through summer 1996 ( x , sd§), Yellowstone National Park, Wyoming.
0
Year/compound+
50
100
Summer
Winter
Summer
Winter
Summer
Winter
1993
Total phenolics
Tannins
Sol. carbo.¤
7141 ± 668
76 ± 10
46 ± 11
4532 ± 1423
48 ± 7a*
35 ± 7
6061 ± 1639
75 ± 11
40 ± 15
4593 ± 847
35 ± 10b
31 ± 3
6649 ± 1793
77 ± 10
46 ± 17
4847 ± 913
47 ± 10a**
23 ± 11
1995
Total phenolics
Tannins
Sol. carbo.
6745 ± 1721
58 ± 12a
32 ± 6
5069 ± 1534
42 ± 12a
26 ± 9
6888 ± 1474
59 ± 21a
30 ± 8
4771 ± 539
46 ± 7a
25 ± 7
7264 ± 1125
79 ± 13b*
31 ± 6
5141 ± 597
62 ± 10b*
25 ± 6
1996
Total phenolics
Tannins
Sol. carbo.
17,166 ± 3343
65 ± 9
47 ± 9a
§
—
—
—
15,265 ± 4864
62 ± 14
25 ± 4b*
—
—
—
16,283 ± 3034
68 ± 12
24 ± 4b*
—
—
Means followed by different letters significantly different at p ≤0.05; p ≤0.10, ANOVA.
Total phenolics expressed as average peak height divided by 100; tannins and soluble carbohydrates expressed as mg/g dry weight.
From S.C. Wooley, M.S. Thesis 1998. Brigham Young University, Provo, UT.
+
¤
trend is associated with a two to three times increase in
phenolic content in the samples taken from Bebb and false
mountain willows (tables 1, 2).
Climate Change, Beaver Abundance,
Ecosystem Processes, and Riparian
Communities
Several factors noted in recent publications indicate a
trend toward aridity and change in habitat quality on the
winter range toward one less suitable for willow growth and
physiological response (table 3) (and perhaps aspen, Romme
et al. 1995). The summer temperature increase has been
0.87°C, while the average January-June precipitation decreased 61 mm. Beaver and their associated activities are an
additional factor affecting water dynamics and ecosystem
processes (table 3). Beaver were found to be almost
USDA Forest Service Proceedings RMRS-P-11. 1999
nonexistent on the winter range in YNP. Their activity
results in local water tables being higher near beaver dams
and surrounding areas, in the formation of a mosaic of
braided, meandering, slow-moving water in streams, and
ponds that are rich and efficient in processing nutrients,
carbon, and litter (table 3) (Naiman and others 1988).
Reduced production, leader length and weight, plant
height, and recruitment of unbrowsed and browsed willows
also suggest poor growing conditions for willows (table 3).
Clipping willows over a 4 year period in YNP exclosures
showed a cumulative negative change in production and
height for the 0, 50, and 100% clipped plants (Singer and
others 1998). Noted also were decreases in catkin production. These, combined with the lack of physiological response
in soluble carbohydrates, low molecular weight phenolics,
and tannins in mechanically clipped willows in exclosures,
suggest that browsing may not be the only factor in willow
declines.
193
Table 3—Verified and predicted parameters describing sites favorable and unfavorable for willow growth, and willow and habitat responses on these
sites, in the northern winter range of Yellowstone National Park, Wyoming.
Site
Parameter/response
Unfavorable
Parameters
Precipitation1-4, 8
Temperature1-4, 8
Water Tables1-3
Streambanks1-3
Flooding1-3
Streams6, 7
Beaver3, 5, 6
Willow Response
Production1-3
Recruitment1-3
Leader Length and Weight1-3
Plant Height1-3
Browsing Effect on Growth Form2
Defense Response
Habitat
Nutrients6, 9
Aquatic Invertebrates6, 7
Carbon6, 7
Litter
Plant Community2, 7, 8
Less, drier winters
Warmer
Higher, wetter
Cooler
Lower
Prevalent downcutting
Common, extensive
Single or few streams, narrow
streams; increased flow
Few to none; loss of food supply
Perennially higher
Less downcutting, vegetated
Infrequent, reduced intensity
Network of braided, expounded streams, ponds;
impounded water, high sediment organic matter
Common; food supply abundant (aspen, willow)
Reduced; negative gain in CAG
Reduced to nonexistent
Short, lighter
Reduced in stature
Morphological juvenility response;
reduced physiological response
Reduced or none
Net increase, vigorous gain in CAG
Seed productivity high, asexual
Longer, heavier
Able to grow beyond reach of elk
Morphological and physiological
juvenility
Induced response vigorous
Reduced input of N
Shredders, scrapers; biomass less
Low carbon input
More recalcitrant; slower processing
Grass, sedges, conifer encroachment,
dryland shrubs
Enhanced N availability
Collectors, predators; greater biomass
High carbon input and processing
More rapidly processed
Mosaic of riparian vegetation; willow
aspen maintained
1
4
7
2
5
8
Singer and others 1998
Singer and others 1994
3
Singer and Cates 1995
Balling and others 1992a,b
Consolo-Murphy and Hanson 1993
6
Naiman and others 1988
9
Naiman and Melillo 1984
Houston 1982
Jonas 1955
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