678
Patterns of willow seed dispersal, seed
entrapment, and seedling establishment in a
heavily browsed montane riparian ecosystem
Edward A. Gage and David J. Cooper
Abstract: Declines in riparian willow (Salix spp.) communities in Rocky Mountain National Park, Colorado, USA ,
coincident with a large increase in elk (Cervus elaphus L.) populations, has raised concerns about the future of willow
communities. To identify possible constraints on willow establishment in two heavily browsed riparian areas, in 2000
and 2001, we examined seed dispersal phenology, germinability, and the spatial patterns of aerial seed rain, quantified
the effects of soil surface relief, texture, and moisture on seed entrapment, and examined natural patterns of seedling
emergence in relation to seed source proximity. All species dispersed seeds following peak streamflow and exhibited
high germination rates (85%–99%). Total seed rain differed between years, although broad spatial patterns were similar.
Seed rain density as high as 7650 seeds/m2 occurred in reference areas but declined by over two orders of magnitude
in heavily disturbed areas and by >90% within 200 m of seed sources. Seed entrapment rates varied significantly with
soil moisture and surface relief, but not with texture, and were low (<30%) regardless of treatment. Seedling density
declined with distance from seed sources, suggesting that propagule availability may limit initial seedling establishment. Without a change in elk population or behavior, or intervention by park managers, degradation of willow communities will likely continue.
Key words: Salix, riparian, dispersal, ungulates, elk.
Résumé : Le déclin des populations ripariennes de saules (Salix spp.), du parc national Rocky Mountain, au Colorado,
USA, qui coïncide avec une forte augmentation des populations de Wapiti (Cervus elaphus L.), soulève des préoccupations au sujet de l’avenir de ces communautés de saules. Afin d’établir des contraintes possibles pour l’établissement
du saule dans deux surfaces ripariennes fortement broutées, en 2000 et 2001, les auteurs ont examiné la phénologie de
la dispersion des graines, le pouvoir germinatif et les patrons spatiaux de la pluie de semence. Ils ont également quantifié les effets du relief de la surface du sol, de la texture et de l’humidité, sur la capture des graines. Ils ont finalement examiné les patrons naturels d’émergence des plantules, en relation avec la proximité des sources de semences.
Toutes les espèces dispersent leurs graines en suivant un flux avec pic, et montrent des taux de germination élevés
(85 % à 99 %). La pluie totale des graines diffère selon les années, bien que les patrons spatiaux généraux soient semblables. Des densités de pluies de graines aussi élevées que 7650 graines/m2 ont pu être observé dans les aires de référence, mais peuvent décliner par un ou deux ordres de grandeur sur les surfaces fortement perturbées, et de plus de
90 %, à moins de 200 m des sources de semences. Les taux de capture des graines varient significativement avec
l’humidité du sol et le relief de surface, mais non avec la texture, et sont très faibles (<30 %) indépendamment du traitement. La densité des plantules décline avec la distance des sources de semences, ce qui suggère que la disponibilité
des propagules pourrait limiter l’établissement initial des plantules. Sans modifications de la population des wapitis, du
comportement ou des interventions des gérants du parc, le déclin des communautés de saules est vraisemblablement appelé à se poursuivre.
Mots clés : Salix, riparien, dispersion, ongulés, wapiti.
[Traduit par la Rédaction]
Gage and Cooper
Introduction
Since the US National Park Service adopted a policy of
natural regulation (i.e., no capture or cull) in the 1960s, elk
(Cervus elaphus L.) populations in Yellowstone and Rocky
687
Mountain National Park have increased dramatically
(Coughenour and Singer 1996; Lubow et al. 2002). During
this period, significant declines in the spatial extent and condition of riparian willow communities has occurred in portions of Rocky Mountain National Park (Peinetti et al.
Received 25 February 2005. Published on the NRC Research Press Web site at http://canjbot.nrc.ca on 6 July 2005.
E.A. Gage and D.J. Cooper.1,2 Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO 80523, USA.
1
Present address: Department of Forest, Rangeland and Watershed Stewardship, Colorado State University, Fort Collins, CO 80523,
USA.
2
Corresponding author (e-mail: davidc@cnr.colostate.edu).
Can. J. Bot. 83: 678–687 (2005)
doi: 10.1139/B05-042
© 2005 NRC Canada
Gage and Cooper
2002), and there is little new willow establishment or recruitment into larger age or size classes, suggesting that the
long-term persistence of these ecosystems is threatened. Although multiple factors may have contributed to the decline,
including climate change, hydrologic changes associated
with declining beaver (Castor canadensis Kuhl) populations,
and direct anthropogenic disturbances (Singer et al. 1998),
intense herbivory associated with a two- to three-fold increase in elk populations since the late 1960s (Lubow et al.
2002) appears to be a principal cause.
Native ungulates can have significant direct and indirect
effects on ecosystems (Frank 1998), although the magnitude
and direction of changes can differ among ecosystem types.
In grasslands, elk increase N-cycling rates, positively affecting primary production (Frank and McNaughton 1993;
Frank and Evans 1997), but the opposite effect has been observed in riparian ecosystems (Singer and Schoenecker
2003). Elk browsing in riparian areas can alter C-cycling
(Menezes et al. 2001), plant water-use patterns (Alstad et al.
1999), and riparian community structure (Singer et al. 1994;
Peinetti et al. 2002). However, one of the most conspicuous
effects is reduced establishment and recruitment of woody
plants, including cottonwood (Populus spp.) (Beschta 2003;
Ripple and Beschta 2003), willow (Salix spp.), and aspen
(Populus tremuloides) (Romme et al. 1995; Suzuki et al.
1999; Ripple and Larsen 2000). Elk browsing can reduce or
eliminate seed production by consuming previous year’s
shoots on which aments would develop (Kay and Chadde
1992; Case and Kauffman 1997; Peinetti et al. 2001). However, the effects of reduced seed production on willow seed
dispersal patterns or seedling establishment are largely unknown.
Willow species share many life history traits (see
Karrenberg et al. 2002), including high initial seed
germinability and rapid decline in seed viability following
maturation (Densmore and Zasada 1982; Krasny et al. 1988;
Van Splunder et al. 1995). Since willows do not form a persistent soil seed bank, seeds must reach bare and moist mineral sediment soon after dispersal for germination and
seedling establishment to occur. Along snowmelt-dominated
rivers, these sediments are typically deposited as the annual
spring flood stage declines, creating habitat for seedling establishment (Karrenberg et al. 2002). Although some willow
species are capable of establishment from asexual
propagules such as beaver-created stem fragments, in the
southern Rocky Mountains such events appear uncommon
(Cottrell 1993, 1995; Dickens 2003).
For wind-dispersed species such as willows, the distance
that propagules move from parent plants to the soil surface,
referred to as primary dispersal, is largely influenced by
seed mass and shape, height of seed release, and the presence of morphological adaptations promoting wind dispersal
(Augspurger and Franson 1987; Greene and Johnson 1989).
The spatial pattern of aerial seed rain is typically leptokurtic,
with seed density peaking near parent plants and rapidly declining with distance outwards (Willson 1992), although the
specific pattern can vary widely among species (Willson
1993).
Redistribution of propagules, or secondary dispersal, can
also influence vegetation patterns, particularly at small
scales (Chambers et al. 1991; Chambers and MacMahon
679
1994; Schupp 1995). Although previous research has
identified a strong relationship between the fate of locally
dispersed seeds and substrate characteristics such as microtopographic relief, soil texture, organic matter content, and
the presence of vegetation (Eckert et al. 1986; Chambers
2000), there is little known about the factors controlling willow seed entrapment (i.e., retention of seeds on substrates
following primary dispersal). Since willow seeds are small,
light, and easily redistributed, factors affecting seed entrapment in suitable microsites may influence initial patterns of
seedling establishment.
Our study goal was to improve our understanding of willow seed dispersal processes and evaluate the hypothesis that
reduced seed production resulting from heavy elk browsing
is limiting willow establishment. Specific objectives included (i) quantifying the spatial and temporal patterns and
processes of aerial willow seed dispersal, (ii) identifying
substrate characteristics influencing rates of willow seed entrapment, and (iii) examining natural patterns of seedling
emergence in relation to seed rain density. In this study, we
did not make direct measurements of elk impacts on willow
communities, but rather analyzed the relationship between
patterns of seed dispersal and initial seedling emergence and
the distribution of seed-producing willows, which in our
study sites is limited by very high levels of elk browsing.
Methods
Study sites
Research was conducted in Moraine and Horseshoe Parks
(elevations of 2480 and 2600 m), two broad, low-gradient
valleys formed behind Pleistocene terminal moraines on the
east slope of Rocky Mountain National Park in Colorado,
USA (Fig. 1). The Fall River, a second-order alluvial stream
in the Big Thompson River watershed, flows east through
Horseshoe Park and exhibits a strongly meandering, poolriffle morphology. The Big Thompson River enters Moraine
Park in the west and, owing in part to extensive historical
beaver activity, splits into a series of distributaries conveying
water across the site, which converge again in the east end of
the valley. Streamflow in both rivers is unregulated, and the
annual, snowmelt-driven peak discharge typically occurs in
late May or early June. Climate is continental, with mean
annual precipitation of approximately 35 cm (Estes Park Station No. 052759, 1948–2001). Peak streamflow on the Big
Thomson River and summer (June–August) precipitation
during the study period were below the long-term average
(63% and 57%, and 83% and 74%, respectively), reflecting
regional drought conditions.
Plant communities are similar in both sites and include
wet and dry meadows supporting a mix of native and introduced grasses, sedges, and herbaceous dicot species, and riparian shrub communities dominated by the willows Salix
monticola (Bebb), Salix geyeriana (Andersson), Salix
bebbiana (Sargent), Salix drummondiana (Barratt), Salix
lucida subsp. caudata (Nutt.) E. Murr, and Salix planifolia
(Pursh) (nomenclature follows Weber and Wittmann 2001).
The westernmost portions of both sites are relatively undisturbed, support dense tall willow stands, and were used as
reference areas for this study. Past recreational and agricultural developments and high levels of elk browsing have se© 2005 NRC Canada
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Can. J. Bot. Vol. 83, 2005
Fig. 1. Locations of Salix spp. seed dispersal studies within Horseshoe Park (A) and Moraine Park (B). Inset boxes (C and D) in Moraine Park denote locations of small-scale seed trap networks. Streamflow in both sites is from west to east.
verely degraded willow communities in central and eastern
Moraine Park, where extremely high winter elk densities,
>90 elk/km2, occur (Singer et al. 2002). Intense browsing
continues to suppress these willows, reducing or completely
eliminating seed production (Peinetti et al. 2001). Willow
density and stature decreases from west to east in Horseshoe
Park as well; however, elk densities are considerably lower
than in Moraine Park (Singer et al. 2002) and seedproducing willows can be found throughout the site (Peinetti
et al. 2002).
Dispersal phenology and seed germination
We monitored the timing of flowering and seed release
weekly from late May through July 2001 for five permanently marked female plants each of S. monticola,
S. planifolia, S. drummondiana, S. geyeriana, S. bebbiana,
and S. lucida subsp. caudata located in reference area willow stands. Plants from both sites were found at similar elevations and topographic settings, occurring on relatively
level floodplains. We collected mature aments from each
species, dried them for 48 h at room temperature to promote
capsule dehiscence, and randomly selected four replicates of
25 seeds each, which we placed on moistened filter paper
under continuous fluorescent light. We assessed germination
over a 10-d period and compared percent germination
among species using a one-way ANOVA following a Tukey–
Kramer multiple comparisons adjustment (Proc GLM in
SAS®; SAS Institute Inc. 2000).
Aerial seed dispersal
We analyzed the timing and spatial pattern of willow seed
dispersal using seed rain traps constructed by mounting 900cm2 plywood squares horizontally above the ground surface.
A total of 60 traps, 20 in Horseshoe Park and 40 in Moraine
Park, were installed at approximately equal distances along a
series of north to south transects (Fig. 1). The principal criterion we used in locating transects was achieving adequate
dispersion of traps across the study areas. In addition, we installed seven traps in willow reference stands, three in Moraine Park and four in Horseshoe Park. To quantify seed
rain, we applied the adhesive Tanglefoot® to the upper surface of traps; we tallied captured seeds and recoated traps
weekly from late May through mid-July 2000 in Horseshoe
Park, and 2000 and 2001 in Moraine Park. Because seeds
from different willow species are visually indistinguishable,
we were unable to separate the contribution of individual
species to seed rain totals. We monitored reference area
traps in both sites during 2000 and 2001 and used a onesided t test to compare mean reference area seed rain density
between years. We used the inverse distance weighted
method in the ArcView® Spatial Analyst extension (ESRI
1999) to interpolate values between traps and generate contour maps of seed rain density. We calculated the distance
from seed traps to the nearest willow seed source using a
modified GIS coverage of willow distribution in the study
areas produced by Peinetti et al. (2002). Based on field observations and results from research exclosures in the study
areas (Peinetti et al. 2001), we determined that only lightly
to moderately browsed willows produced seed; we found no
plants outside of exclosures that did not exhibit some degree
of past browsing. To evaluate broad-scale changes in seed
rain density across the study areas, we conducted a nonlinear
regression of cumulative seasonal seed rain versus the distance from the trap to seed-producing willow stands using a
negative exponential function (Sigmaplot®; SPSS 2002).
To quantify seed rain attenuation rates at finer spatial
scales, 95 additional seed rain traps were installed during
2001 at 7-m intervals along a total of 12 transects originat© 2005 NRC Canada
Gage and Cooper
ing at the base of two isolated seed-producing willow
patches and oriented along major compass lines (Fig. 1). Because of strong prevailing westerly wind patterns and the
presence of additional willow stands to the west of these
study patches, we focused our analyses on the 41 traps
found in the three east-trending transects. Nonlinear regression was used to relate log+1 transformed seed rain density
(y, in seeds/m2) to the distance (x, in m) from seed producing willow patches. We fit a negative exponential function
(Willson 1992; Nathan et al. 2000) to transect data using
Sigmaplot® (SPSS 2002).
Willow seed entrapment
To evaluate the effects of microtopographic relief, soil
texture, and soil moisture on rates of willow seed entrapment, which we defined as the percentage of seeds retained
on a soil’s surface following initial seed contact, we established a split-plot factorial experiment in a flat meadow area
adjacent to the Big Thompson River in Moraine Park. In
each of five replicates, six cylindrical vinyl trays, 18 cm in
diameter and 5 cm deep, were buried flush with the ground
surface and filled with one of two homogenized soil types:
coarse sand from point bars or loamy sand excavated from a
beaver pond. Trays were randomly assigned one of three
surface relief treatments (high, medium, or low), intended to
represent the surface relief characteristics of natural fluvial
landforms such as point bars or abandoned beaver ponds. To
create different relief treatments, we placed 2.6 cm tall wood
cubes on the tray surface to cover approximately 0%, 30%,
or 60% of the total surface area (Fig. 2). Two trials, wet (saturated soils) and dry (soils initially at field capacity and allowed to dry over the sampling period), were run to evaluate
the effect of different soil moisture levels on entrapment
rates.
In each trial, S. monticola seeds, which are morphologically indistinguishable from the seeds of other willow species present in the study area, were dropped individually
through a 30 cm tall cylinder and allowed to settle onto the
surface of each tray. The cylinder was then carefully removed and the number of seeds remaining on the tray surface was counted after 3 h, and again after 30 h (the
approximate time required to initiate seed germination in our
viability trials). The entrapment rate was calculated as the
number of seeds present at each time step divided by the
number of seeds added. To evaluate treatment effects on
rates of seed entrapment, we analyzed the 30-hour entrapment data for the combined dry and wet trials using
ANOVA. We initially analyzed the full model, including all
main factors and interaction terms. However, because the
soil texture main effect and associated two- and three-way
interactions were not significant, plots from the two soil textures were pooled and the analysis rerun. Pairwise comparisons among treatment means were made using this model
following a Tukey–Kramer multiple comparison adjustment
(Proc GLM in SAS®; SAS Institute Inc. 2000).
Natural patterns of willow seedling establishment
In 2001, we analyzed natural willow seedling emergence
along the main channel of the Big Thompson River in Moraine Park. Using a global positioning system (GPS) unit
and aerial photographs, we mapped all point bars found
681
Fig. 2. Schematic diagram illustrating split-plot design used for
Salix spp. seed entrapment experiment, with soil texture and surface roughness treatments nested within moisture treatments.
along the river. We randomly sampled seven of these within
each of four stream reaches of approximately equal length
(Fig. 1). On each bar selected for sampling, we used stage
measurements from local staff gauges to estimate the area
available for seedling establishment, assumed to be the area
exposed during the period of active seed rain. We then sampled current-year seedlings using a series of continuous
0.25-m2 quadrats placed along lines oriented perpendicular
to the main axis of the point bar. Lines ran from the edge of
perennial vegetation to the edge of the bar that was available
for colonization during the seed rain period and were spaced
at 2-m increments along the point bar’s main axis. Nonlinear
regression using a negative exponential model was used to
relate the mean seedling density calculated for each bar to
distance from seed-producing willow patches.
Results
Dispersal phenology and seed germination
In 2001, Salix planifolia was the first species to initiate
dispersal, beginning in late May, while S. lucida subsp.
caudata, a relatively uncommon species, was the last to
complete seed release, in mid-July (Fig. 3). The highest seed
rain densities occurred when aments of S. monticola and
S. geyeriana, by far the two most abundant species in the
study areas, matured during early June through early July.
The timing of seed release corresponded with the timing of
river stage decline (Fig. 3).
Nearly all seeds analyzed initiated germination within
72 h after being placed onto moistened filter paper, and percent germination was high for all species (S. monticola 99%,
S. bebbiana 97%, S. lucida subsp. caudata 95%,
S. geyeriana 91%, and S. planifolia 85%). There were no
significant differences in germination rates among species
with the exception of S. planifolia, which had significantly
lower germinability than S. monticola (p = 0.003) and
S. bebbiana (p = 0.021), but not S. geyeriana (p = 0.492) or
S. lucida subsp. caudata (p = 0.07).
Aerial dispersal of willow seeds
The highest seed rain densities in both years occurred in
the reference areas in the western portion of the study sites.
The maximum cumulative seed rain density in Moraine Park
during 2000 was 7650 seeds/m2 versus 3850 seeds/m2 in
2001. The maximum seed rain density in the Horseshoe Park
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Can. J. Bot. Vol. 83, 2005
Fig. 3. Mean daily Salix spp. seed rain during 2001 (solid line) for reference area seed rain traps, calculated by dividing weekly seed
rain totals by the number of days between trap readings, plotted against mean daily flow of the Big Thompson River (USGS gauge
No. 06733000) during the 2001 field season (dotted line) and for the period 1946–1998 (dashed line). Horizontal bars illustrate approximate period of seed release for the most abundant willow species in the study area.
Fig. 4. Cumulative annual Salix spp. seed rain in Moraine and Horseshoe Parks for the 2000 season. Contour lines in Moraine Park
are at intervals of 50 seeds/m2, with the exception of the central portion, where lines represent 25 seeds/m2. Contour lines in Horseshoe Park are at intervals of 100 seeds/m2.
© 2005 NRC Canada
Gage and Cooper
Fig. 5. Cumulative annual Salix spp. seed rain plotted against
distance to seed-producing willows. (A) Horseshoe Park (log(y) =
1.9 + 1.55 × e(–0.0347x), n = 20, r2 = 0.82, p < 0.0001).
(B) Moraine Park (log(y) = 1.32 +1.82 × e(–0.0097x), n = 39, r2 =
0.74, p < 0.0001). (C) East-trending fine-scale seed rain trap
transects in Moraine Park (log(y1) = –0.468 + 2.46 × e(–0.0123x), n =
10, r2 = 0.76, p = 0.006; log (y2) = –49.53 + 52 × e(–0.0002x), n =
15, r2 = 0.895, p < 0.0001; log (y3) = –100.18 + 102.68 × e(–0.0001x),
n = 16, r2 = 0.82, p < 0.0001). Note use of log scale for y-axes
in Figs. 5A and 5B and the different scales for x-axes among
plots.
reference area was similarly high, 5025 and 3750 seeds/m2
in 2000 and 2001. The mean seed rain density in 2000 for
all reference area traps, 4466 seeds/m2, was significantly
683
greater than the 2001 density of 2589 seeds/m2 (t = 2.03, df =
10, p = 0.035), indicating high inter-annual variability in
seed production.
The spatial patterns of seed rain were different between
sites. In Moraine Park, seed rain density decreased by more
than two orders of magnitude from west to east, and >70%
of the site received seed rain densities ≤0.1% of reference
area values (Fig. 4). An exception to this trend occurred in
far eastern Moraine Park, where a small peak in seed rain
was observed near an isolated seed-producing willow stand
associated with a sloping fen (Fig. 4). Cumulative annual
seed rain was negatively correlated (n = 39, p < 0.0001, r2 =
0.74) with distance from seed-producing willows, with
>90% of total seed rain observed within 200 m of seed
sources (Fig. 5). However, all traps except one captured at
least one seed during the 2-year study period, suggesting
that a very low background level of seed rain reaches most
of the study areas. In Horseshoe Park, the highest seed rain
density occurred in the far west, while the lowest seed rain
densities occurred in the central and far eastern portion of
the study area (Fig. 4). Seed rain density was also negatively
correlated with distance from seed-producing plants in
Horseshoe Park (n = 20, p < 0.0001, r2 = 0.82; Fig 5). However, in contrast to Moraine Park, seed-producing plants occur in several patches throughout the site, creating localized
peaks in seed rain density (Fig. 4). In particular, a large sloping fen reaches the valley floor in the central portion of
Horseshoe Park and supports a large willow population that
is apparently less browsed than willows in adjacent communities.
Finer-scale analyses indicated that a rapid decrease in
seed rain density occurs with increasing distance from seedproducing willows. Parameter estimates from a nonlinear regression of log+1 transformed seed rain density values (y)
against distance, in metres, from patch edge (x) for the three
east trending transects were variable, but all functions had
relatively steep slopes and showed a strong fit to the data.
Seed rain distributions exhibited a leptokurtic form, with
peak densities occurring within 15 m of the patch edge
(Fig. 5). More than 50% of the cumulative seed rain along
these transects occurred within 30 m of the willow patch
edge. Only weak trends occurred along transects oriented in
directions other than east, likely owing to strong prevailing
westerly winds and the influence of nearby seed-producing
patches. Even among the east-trending transects, there was
considerable variability in total seed rain density, likely owing to differences in fecundity among willows near the origin of transect lines (Fig. 5).
Willow seed entrapment
Mean willow seed entrapment rates ranged from approximately 2% to 30% over the 30-h sample period (Fig. 6).
High relief treatments trapped more seeds than low relief
treatments for both moisture treatments (Fig. 6). The percentage of retained seeds declined between the 3- and 30-h
measurements in both trials, but at a greater rate in the dry
(49.5%) than in the wet (19.9%) trial. In general, higher entrapment rates were observed in the wet trial, although the
magnitude of the moisture effect was influenced by the level
of relief, as indicated by the statistically significant interaction between the moisture and relief terms (Table 1).
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Can. J. Bot. Vol. 83, 2005
Fig. 6. Mean percent Salix monticola seed entrapment (±1 SEM)
in dry and wet treatments with low, medium, and high relief
treatments. Data for plots with different soil textures were pooled
for each surface relief and moisture combination. Treatments not
sharing letters are significantly different (ANOVA, α = 0.05).
Table 1. Results from ANOVA of 30-h Salix monticola seed entrapment data, pooled over soil textures.
Treatment
df
MSE
F value
P
Model
Error
Corrected total
Relief
Moisture
Relief × moisture
5
54
59
2
1
2
10.75
0.82
—
11.88
22.32
3.82
13.04
—
—
14.41
27.09
4.63
<0.0001
—
—
<0.0001
<0.0001
0.0139
Natural patterns of willow seedling establishment
The highest mean seedling densities on point bars occurred in western Moraine Park reference areas. Mean seedling density decreased with distance from seed-producing
willow stands, and a negative exponential model showed a
reasonable fit to the data (n = 27, p < 0.0001, r2 = 0.58;
Fig. 7). Seedling distribution on individual point bars was
highly variable, with approximately 65% of plots containing
no willow seedlings.
Discussion
The high seed rain density in our reference areas is likely
typical of mature, lightly browsed willow stands in our study
region. The high inter-annual variability in total seed rain is
also probably typical, as both seed production and release
are influenced by weather conditions. Aments appear in the
early spring and can be killed by freezing temperatures, depressing seed production. In addition, seed release and dispersal are likely influenced by periods of rain.
Fig. 7. Mean Salix spp. seedling density on point bars plotted
against distance from nearest seed-producing willow patch. The
dashed line represents the best-fit nonlinear regression line (y =
3.66 × e(–0.023x) + 0.25, r2 = 0.58, p < 0.0001).
In contrast to reference areas, there was little or no seed
production in heavily browsed central and eastern Moraine
Park, and to a lesser extent, the central and eastern portions
of Horseshoe Park. The effects of heavy browsing on willow
seed production have been demonstrated in experimental animal exclosures in riparian areas of the Pacific Northwest
(Case and Kauffman 1997; Brookshire et al. 2002) and
Rocky Mountain regions of the USA (Kay and Chadde
1992; Peinetti et al. 2001). Because browsing removes
leaves as well as stems on which aments would be produced,
flower and seed production is reduced or eliminated. Our results suggest that such sustained, intense browsing has a profound effect on the spatial distribution and abundance of
willow seeds, reducing the probability of seeds reaching
suitable sites for germination. Although hydrochory (i.e.,
dispersal by water) has the potential to transport seeds to areas lacking seed-producing plants (Nilsson et al. 1991;
Merritt and Wohl 2002), we found no evidence, such as seed
drift lines or rows of seedlings along stream margins, to suggest that hydrochory can compensate for low aerial seed rain
densities in our study areas.
Our small-scale trap data indicate that seed rain density
declines sharply with distance from parent plants. The strong
leptokurtic distribution that we observed is consistent with
previous work on other wind-dispersed species (Willson
1993; Nathan et al. 2001). Although willow seeds have small
mass and are well adapted for aerial transport, we measured
an approximately 90% reduction in seed rain density within
200 m of parent plants. The restricted distribution of seedproducing plants, coupled with the limited dispersal distance
of most seeds, explains the two orders of magnitude decline
in seed rain density from reference stands to the central and
eastern portions of Moraine Park, where impacts from elk
are most pronounced. The more variable pattern observed in
Horseshoe Park is likely due to the much lower winter elk
densities relative to Moraine Park (Singer et al. 2002), al© 2005 NRC Canada
Gage and Cooper
lowing some willow stems to escape browsing each year and
aments to develop.
The timing of maximum willow seed rain in our study areas coincided with peak stream discharge and the period of
rapidly decreasing flows, a pattern that has been documented
for willows in other regions (Niiyama 1990) and for related
genera such as Populus spp. (Cooper et al. 1999). We also
documented high seed germination rates, as typically occurs
with most willow species (Krasny et al. 1988; Van Splunder
et al. 1995). This suggests that neither the timing of dispersal nor seed viability are the primary constraints on initial
seedling establishment, and the scarcity of willow seedlings
in much of the study area is due to other factors.
The low seed entrapment rates that we measured indicate
that primary dispersal measurements, such as those from our
sticky traps, overestimate effective dispersal rates. The importance of secondary dispersal has also been shown for
halophytes in a California playa where low seed entrapment,
rather than low propagule supply, limited seedling establishment (Fort and Richards 1998). Studies in alpine tundra
(Chambers et al. 1991, Chambers 1995), grasslands (Peart
and Clifford 1987; Aguiar and Sala 1997), and shrub–steppe
ecosystems (Chambers 2000) have also demonstrated important seed entrapment effects on community development.
The significant influence of both soil moisture and relief on
seed entrapment in our study suggests that differential seed
entrapment rates result from the unique topographic,
hydrologic, and edaphic characteristics of floodplain landforms, such as point bars, ox-bows, and abandoned beaver
ponds, and may help explain differences in willow establishment patterns among landforms (Dickens 2003). For example, fine-textured sediment typically found in abandoned
beaver ponds has high water-holding capacity, which should
facilitate entrapment, but the soil surface has little microtopographic relief, which likely reduces seed entrapment
rates. In contrast, point bars along high-energy streams typically have gravel or cobble substrates. Their much larger
clasts, ranging from several millimetres to >10 cm in diameter, offer relatively high microtopographic relief but little
water holding capacity. Although such features may promote
seed entrapment, they may not be conducive to seed germination and seedling survival, suggesting that multiple factors
interact to determine small-scale recruitment patterns (Houle
1992; Schupp 1995).
The declining density of willow seedlings that we observed with increasing distance from seed-producing plants
suggests that seed availability constrains initial seedling
emergence. Nathan et al. (2000) suggested that low seed dispersal rates for Pinus halapensis, at distances of as little as
20 m from parent plants, limited establishment despite the
production of large seed crops. Although willow seeds are
much lighter and have greater mean dispersal distances than
species of Pinus, a similar effect is certainly possible. An alternative hypothesis, that herbivory of seedlings by elk limits
first-year seedling establishment in our study area, appears
unlikely because most elk migrate to subalpine and alpine
tundra ecosystems during the summer, and first-year seedlings are very small, <10 cm tall, and not an apparent food
source. We also found no evidence of systematic trends in
trampling effects from elk or recreational users or in the
685
characteristics of fluvial landforms, such as sediment caliber, across our study area that might explain these patterns.
Elk herbivory and trampling, flood driven erosion, or beaver herbivory or inundation from beaver activities may limit
survival of older willow plants. However, patterns of seed
rain, seed entrapment, and germination create the initial template of seedlings subsequently affected by geomorphic and
ecological processes, and thereby influence where and in
what abundance recruitment can occur. Willow seedling cohorts typically experience mortality rates of 80%–100% because of desiccation (Sacchi and Price 1992) and flood scour
(McBride and Strahan 1984; Gage and Cooper 2004a), and
landforms suitable for germination occupy a very small portion (<2%) of the study area landscapes. Consequently, factors that further reduce the likelihood of new establishment,
such as inadequate propagule supplies, may have long-term
impacts on willow community development and persistence
on the landscape.
Our analyses indicate that willow seed rain patterns are
strongly influenced by the distribution of seed-producing
plants. Although we did not directly measure levels of elk
herbivory, previous research in our study sites has directly
linked reduced willow stature and seed production to anomalously high levels of elk browsing (Peinetti et al. 2001).
Where browsing intensity is high, as it is in most of our
study area, nearly all shoots from the previous year are consumed. This results in the production of few aments and severe reductions in willow seed rain density over broad areas.
These results add to the substantial body of research suggesting that high elk populations, as occurs in National
Parks such as Yellowstone and Rocky Mountain, can have
major impacts on woody browse species including willows
(Peinetti et al. 2002; Ripple and Beschta 2003; Ripple and
Beschta 2004a). In Yellowstone, behavioral and lethal effects from reintroduced wolves may limit elk browsing in
some riparian areas (Beschta 2003; Ripple and Beschta
2004b), improving chances for long-term recovery of degraded communities. However, because elk in Rocky Mountain National Park lack predators, there appears to be no
effective constraint on browsing.
Without a reduction in elk population size, changes in
their behavior, or intervention by managers to limit elk access to willow stands, the degradation of riparian willows
will likely continue. Ongoing loss of willows because of
heavy browsing, along with low establishment and recruitment rates, could result in the transformation of shrubdominated riparian communities into herbaceous-dominated
ones, resulting in the loss of important ecological functions.
To increase the short-term prospects for willow establishment in Rocky Mountain National Park, we suggest that existing willow stands be protected from herbivory using
fences where necessary and new willow populations be established by planting cuttings (Gage and Cooper 2004b) or
seedlings to create new loci for seed production, especially
in areas that receive little seed rain.
Acknowledgements
This research was supported by the National Park Service
Water Resources Division and Rocky Mountain National
© 2005 NRC Canada
686
Park. Additional support was provided by a Society of Wetland Scientists student research grant. Support by Rocky
Mountain National Park staff is gratefully acknowledged, especially T. Johnson, R. Monello, and R. Thomas. Thanks to
D. Merritt and P. Chapman for guidance with statistical
analyses and to J. Dickens, R. Inglis, and S. Woods for assistance in the field. Thanks also to D. Binkley, D.
Steingraeber, P. Kotanen, R.L. Peterson, and two anonymous reviewers for valuable comments on the manuscript.
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