Scale and plant invasions: a theory of biotic acceptance
Měřítko studia a rostlinné invaze: teorie biotické akceptance
Thomas J. S t o h l g r e n1
, Catherine J a r n e v i c h1
, Geneva W. C h o n g2
& Paul H. E v a n g e l i s t a3
D e d i c a t e d t o M a r c e l R e j m á n e k
1
Fort Collins Science Center, U. S. Geological Survey, 2150 Centre Street, Building C, Fort
Collins, CO 80526, USA, e-mail: tom_stohlgren@usgs.gov; 2
Northern Rocky Mountain Science
Center, U. S. Geological Survey, 675 E Broadway, Jackson, WY 83001, USA; 3
Natural
Resource Ecology Laboratory, Colorado State University, Fort Collins, CO 80523, USA
Stohlgren T., Jarnevich C., Chong G. W. & Evangelista P. H. (2006): Scale and plant invasions:
A theory of biotic acceptance. ­ Preslia 78: 405­426.
We examined the relationship between native and alien plant species richness, cover, and estimated
biomass at multiple spatial scales. The large dataset included 7051 1-m
2
subplots, 1443 10-m
2
subplots,
and 727 100-m2
subplots, nested in 727 1000-m2
plots in 37 natural vegetation types in seven
states in the central United States. We found that native and alien species richness (averaged across
the vegetation types) increased significantly with plot area. Furthermore, the relationship between
native and alien species richness became increasingly positive and significant from the plant neighbourhood
scale (1-m
2
) to the 10-m
2
, 100-m
2
, and the 1000-m
2
scale where over 80% of the vegetation
types had positive slopes between native and alien species richness. Both native and alien plant
species may be responding to increased resource availability and/or habitat heterogeneity with increased
area. We found significant positive relationships between the coefficient of variation of native
cover in 1-m
2
subplots in a vegetation type (i.e. a measure of habitat heterogeneity), and both
the relative cover and relative biomass of alien plant species. At the 1000-m
2
scale, we did find weak
negative relationships between native species richness and the cover, biomass, and relative cover of
alien plant species. However, we found very strong positive relationships between alien species
richness and the cover, relative cover, and relative biomass of alien species at regional scales. These
results, along with many other field studies in natural ecosystems, show that the dominant general
pattern in invasion ecology at multiple spatial scales is one of "biotic acceptance" where natural
ecosystems tend to accommodate the establishment and coexistence of introduced species despite
the presence and abundance of native species.
K e y w o r d s : alien species dominance, biotic acceptance, diversity and invasibility, exotic plant
species, multi-scale sampling.
Introduction
Observational studies, controlled experiments, and theoretical models have been used to
investigate the role of diversity in inhibiting invasions. The prevailing paradigm was based
largely on observations that low diversity islands were easily invaded (i.e. with greatly reduced
environmental gradients and levels of habitat heterogeneity, Elton 1958), and reinforced
by the immensely successful invasions of alien plants and animals on Guam and the
Hawaiian Islands (Mack et al. 2000). However, different environmental characteristics of
islands produced different levels of plant invasions, with tropical islands being more
heavily invaded than islands in temperate zones (Rejmánek 1996). Because islands also
Preslia 78: 405­426, 2006 405
varied in distances from the mainlands, area, and habitat heterogeneity, generalizations
were slow to emerge, especially for largely ignored continental areas (Rejmánek 1996,
Chytrý et al. 2005, Stohlgren et al. 2005b, Richardson & Pyšek 2006).
Contradictory field observations at different spatial scales (i.e. scales of observations,
plot size) have contributed to the confusion. For example, Stohlgren et al. (1999) reported
that four grassland vegetation types in the central grasslands biome in the US showed negative
relationships between native and alien species richness at 1-m2
and 1000-m2
scales,
while five vegetation types in a montane biome of Colorado showed positive relationships
at the same two spatial scales. These findings and other contradictory site-specific studies
underscore the dire need for additional multi-scale studies of native and alien plant species
patterns (Fridley et al. 2006).
Small-scale, controlled experiments of artificially constructed "communities" (Knops
et al. 1997, Tilman 1997, Kennedy et al. 2002) generally supported the "biotic resistance"
paradigm whereby species-rich habitats would be less prone to invasion than species-poor
habitats, presumably due to competitive exclusion (Grime 1973) and by usurping available
resources (Tilman 1997). Likewise, small-scale experiments supporting biotic resistance
have been corroborated by some theoretical studies (Case 1990). Shea & Chesson
(2002) presumed negative relationships between native and alien species within speciespoor
habitats and species-rich habitats at small spatial scales, where extrinsic factors do
not vary, but a positive relationship across habitats, where extrinsic factors do vary. One of
many implicit assumptions of small-scale studies is that the patterns and processes observed
in small plots are directly scalable to larger areas (Fridley et al. 2006). For example,
after a series of small-scale experiments Kennedy et al. (2002) proclaimed that "diverse
communities will probably require minimal maintenance and monitoring because they are
generally effective at excluding undesirable invaders." Fridley et al. (2004) used null models
and multi-scale plot data in one area to show that the relationship between native and
alien species richness may be positive at small and large scales, but it was more positive at
larger spatial scales (also see Brown & Peet 2003). Unfortunately, the null models of
Fridley et al. assumed "uniform random selection of species" (i.e. random community assembly)
in a small species pool of 20 to 100 species, a constant proportion of species by
origin (75% native, 15% exotic, and 10% "blank" species or open spaces), a constant plant
density, equilibrium abundance (sensu Hubbell 2001), and equal-sized individuals regardless
of species and age; conditions that are rarely if ever found in nature. Thus, direct comparisons
of observational studies to these types of null models are problematic (also see
Huston 1997).
Issues of scale have been embraced by observational ecologists as a means of documenting
patterns of invasion at local, regional, and national scales (Stohlgren et al. 1999,
2003, 2005b, Sax 2002, Brown & Peet 2003, Fridley et al. 2006). As a result, some consistent
patterns are emerging. At sub-continental scales, for example, there is convincing evidence
of strong positive relationships between native and alien plant species richness
(Stohlgren et al. 2003), and for plant, bird and fish species in the conterminous United
States (Stohlgren et al. 2005a, 2006). These results complement landscape-scale observational
studies (e.g., Stohlgren et al. 1999, Brown & Peet 2003, Keeley et al. 2003), but they
do not provide a mechanism for the observed patterns across scales (Levine et al. 2003,
2004). Still, there have been no studies to examine the continuum of relationships between
native and alien species from the scale of meters to regions and across many vegetation
406 Preslia 78: 405­426, 2006
types and biomes. Questions remain about how typical positive or negative relationships
between native and alien species are at small spatial scales, and about how the relationships
change with increasing scale and within and across vegetation types.
Having gathered consistent, multi-scale data in many areas in the central US, we had
a unique opportunity to quantify the relationship between native and alien species at six
spatial scales from 1-, 10-, 100-, and 1000-m2
scales, at landscape scales, and for the region.
Our objective was to quantify the relationship between native and alien species richness,
cover, and biomass at multiple spatial scales and for many vegetation types. Increases
in native and alien richness across scales may suggest that similar mechanisms affect
both native and alien plant species.
Study areas
This is the first regional synthesis of our past landscape-scale studies and those of other investigators
that used the modified-Whittaker multi-scale sampling design (described below).
Primary study sites included Rocky Mountain National Park, Colorado, and the
Grand Staircase-Escalante National Monument, Utah (Fig. 1, Appendix 1), with secondary
sites scattered across the central United States.
The 108,000 ha Rocky Mountain National Park is characterized by mountainous geography
spanning elevations from 2500­4345 m with diverse vegetation including meadows,
montane pine and fir forests, subalpine forests and alpine tundra (Fig. 1, Lee 2001).
The Park contained 181 vegetation plots sampled between 1993 and 2001 (Chong 2002).
Stohlgren et al.: Scale and plant invasions 407
Pipestone NM
Tallgrass Prairie
Ponderosa Pine
Wind Cave NP
Mixed Grass Prairie
Wild Horse NWP
Cushion Plant
Yellowstone N.P.
Wet Meadow
Charles Russell NWR
Northern Mixed Prairie
Shortgrass Steppe
Riparian, Sage
Bighorn Canyon NRA
N. Mixed grass
Riparian
Old Aspen
Mixed grass
Grand StaircaseEscalante
NM
Desert Shrub
Desert Mixed Grass
Rabbitbrush Sage
Blackbrush Juniper
Desert Shortgrass
Pinyon Pine
Pinyon-Juniper
Pinyon-Juniper-Manzanita
Pinyon-Juniper-Oak
Pinyon-Juniper-Sage
Aspen
Spring Wet Meadow
Perennial Riparian
Mountain Shrub
Rocky Mountain N. P.
Tundra
Subalpine Limber Pine
Spruce Fir
Lodgepole Pine
Douglas Fir
Ponderosa Pine
Willow
Wet Meadow
Dry Meadow
Aspen
Fig. 1. ­ General map of the vegetation types surveyed between 1993­2004 (see also Appendix 1).
The 850,000-ha Grand Staircase-Escalante National Monument, Utah includes tablelands
of the Colorado Plateau, arid grasslands and shrublands, sparse to closed woodlands,
and large and small patches of forests (Comstock & Elhleringer 1992). The area contains
a wide array of desert shrub, pinyon-juniper, and riparian vegetation types (Fig. 1, Appendix
1), endemic species, hot spots of native plant diversity amid arid, stressful environments,
and multiple exposed soil and geology types (Comstock & Elhleringer 1992,
Shultz 1998, Stohlgren et al. 2005b). Field sampling occurred between 1998 and 2002
(see Stohlgren et al. 2005b for details).
Another 159 plots were established at secondary study sites in various states, biomes,
and vegetation types using the same field methods (i.e. modified-Whittaker plot) in each
vegetation type. Plots were located from tallgrass prairie in Minnesota, to mixed grasslands
and forests in Montana, Wyoming, South Dakota, and Colorado. These other sites
ranged in elevation from 500 m to over 3000 m, in a wide range of geologic and soil types
(Appendix 1).
Methods
In each study location, and during peak phenology, modified-Whittaker multi-scale plots
(Stohlgren et al. 1995, 1998a) were established initially in 48 different vegetation associations.
The nested plot was 20 m × 50 m containing one 100-m2
subplot (5 m × 20 m) in the
center, two 10-m2
subplots (2 m × 5 m) in opposite corners, and ten 1-m2
subplots (0.5 m ×
2 m) systematically arranged around the inside edges of the 1000-m2
plot and the outside
edges of the 100-m2
subplot. Foliar cover (nearest percent) and average height by plant
species were recorded in the ten 1-m2
subplots, along with the percent cover of soil, litter,
bare soil, and rock. Plant species were recorded as 0.5% cover if they occupied less than
1% in a 1-m2
subplot. For more details see Stohlgren et al. (1995, 1998a). The dominance
of aliens in a plot was expressed as the relative cover (percent of total cover) or the relative
biomass (percent of total biomass) of alien species. Cumulative plant species presence was
recorded in the 10-, 100- and 1000-m2
plots. Ancillary data included the slope and aspect
of the plot, GPS location and elevation derived from a digital elevation model.
Statistical approach
We used detailed information on foliar cover and height by species on 7042 1-m2
subplots
to create an index of aboveground biomass by multiplying foliar cover times mean plant
height for native and alien species. Previous research relating cover and height to plant
biomass for Bromus tectorum showed that foliar cover, predicted biomass (cover ×
height), and actual biomass (clipped, dried, and weighed samples) were highly positively
related (R2
> 0.80, Waters 2003). We lacked actual biomass information for other species,
but we concluded that biomass estimates were a better measure of dominance than foliar
cover or height measurements alone when comparing wildly different vegetation types
(tundra to tallgrass prairie, thick conifer forests to desert grasslands).
Linear and non-linear regression analyses (SYSTAT version 11.0) were used to relate
native and alien plant species richness at the 1-, 10-, 100- and 1000-m2
scales, and when
plots were combined within vegetation types. In all analyses described below, data were
408 Preslia 78: 405­426, 2006
log-transformed (log10 x+1) prior to analyses to improve normality. Due to small sample
sizes or high species overlap among types, the 48 original vegetation associations surveyed
were collapsed into 37 vegetation "types" for all analyses (Fig. 1, Appendix 1).
Still, the study encompassed a wide range of environments across seven states (Appendix
1 and 2). Because the number of 1000-m2
plots varied greatly by vegetation type, we summarized
the data as mean values of vegetation characteristics by vegetation type (Appendix
2). This minimized the effect of unequal sampling in different vegetation types and
more accurately represented regional patterns. We did not have the aerial coverage of vegetation
types across the region to aerially weight the results. Still, this approach provides
direct comparisons to the primary studies cited in the Introduction (e.g., Brown & Peet
2003, Keeley et al. 2003, Bruno et al. 2004). We evaluated whether high native species
richness would be positively associated with alien species richness, cover, and biomass at
multiple spatial scales.
We further evaluated whether the cover, estimated biomass, relative cover, and relative
biomass of alien plant species would be positively related to alien species richness for the
vegetation types surveyed. Based on preliminary results (Stohlgren et al. 1999, 2001), we
suspected that habitats vulnerable to the establishment of several alien plant species would
eventually be invaded by a high-biomass producing alien species (Huston 1997).
We evaluated the relationship of native to alien species richness at the vegetation type
scale using the cumulative native and alien species in each type. We assumed this to be
a simple index of the proportional diversity of native and alien species in a type regardless
of sample size. For example, aspen plots in Colorado contained 377 native species and 35
alien species in 45 plots, while the pinyon-juniper type in Utah contained 252 native species
and 16 alien species in 114 plots.
Lastly, we used the coefficient of variation in the foliar cover of native species in all 1-m2
subplots in each vegetation type as a measure of habitat heterogeneity at the plot and vegetation-type
scales. We suspected that a high coefficient of variation in foliar cover of native
species, as an index of habitat heterogeneity, would be positively associated with the level
of establishment and dominance of alien plant species in a vegetation type, as indicated by
high richness, relative cover, and estimated biomass of alien species in a vegetation type.
Results
Multi-scale plot results
Mean native species richness varied greatly among vegetation types ranging from 1.9 to
13.9 species in 1-m2
subplots in spring-desert vegetation in Utah and high-elevation tundra
in Colorado, respectively. These same two vegetation types each had about 38 species per
1000-m2
plot (Appendix 2). Mean alien species richness among vegetation types ranged
from zero alien species in 1-m2
subplots in four vegetation types to a mean of 10 alien species
per 1000-m2
plot in the irrigated shortgrass steppe type in southern Colorado.
The mean understory foliar cover of native and alien plant species also varied considerably
among vegetation types (Appendix 2). Mean foliar cover per plot for native plant species
ranged from 89% cover in aspen stands in Colorado to just 13% cover for the desert
shrub type in Utah. For alien plant species, mean foliar cover was near zero for tundra plots
Stohlgren et al.: Scale and plant invasions 409
(with a very occasional Taraxacum officinale) to 32%, again for the irrigated shortgrass
steppe in Colorado (Appendix 2).
The multi-scale plot design allowed for a cursory comparison of the slopes of the relationship
between native and alien plant species richness at various scales within vegetation
types. While the slopes (and significance of slopes) varied widely by scale (i.e. 1-m2
, 10-
m2
, 100-m2
, and 1000-m2
scales) and vegetation type, we found that 60% of the vegetation
types had positive relationships between native and alien species richness at the 1-m2
scale, and 15 vegetation types had positive slopes at all four spatial scales. Only two vegetation
types, the sagebrush type in Colorado and the recently burned pinyon-juniper sage
type, had negative slopes at all four spatial scales. When we looked across vegetation
types, we found a consistent, progressive pattern whereby the percentage of vegetation
types with positive relationships between native and alien species richness increased with
increasing spatial scale. At the 1000-m2
scale, about 19% of the vegetation types had negative
relationships, while 81% of the vegetation types surveyed had positive relationships.
We found that both the slope and intercept of the relationship between native species
cover and richness consistently increased across the four spatial scales (Table 1). All the
relationships were highly significant and the correlation coefficients increased with spatial
scale. However, the relationship between alien species richness and native species cover
was trending negative at the four spatial scales, but it was only statistically significant at
the 1-m2
scale. There was a consistent increase in the intercept, combined with the consistent
decline in the correlation coefficient (and significance level) with increasing spatial
scale (Table 1).
When we evaluated the mean slope of the relationship between native and alien species
richness, averaged across the 37 vegetation types, we found a significantly increasing positive
slope with increasing spatial scale (Fig. 2). The polynomial model was a better fit than
a linear model. In addition, the coefficients of variation on the slope steadily decreased for
the 1-m2
, 10-m2
, 100-m2
, and 1000-m2
scales, respectively. The mean slope for the vegetation
types was negative (­0.002), but near zero for the 1-m2
scale, and was significantly
different from zero at the 100-m2
and 1000-m2
scales. The proximate reasons for the
increasing positive slope in Fig. 2 were: (1) native species richness (averaged across the
vegetation types) increased significantly and quickly with plot area (x) where native species
richness = 2.4x2
+ 0.63x + 5.57 (R2
= 0.75; n = 37; P < 0.0001 vegetation types for four
plot sizes); (2) alien species richness increased significantly, but slowly, with plot area (x)
where alien species richness = 0.27x2
­ 0.08x + 0.61 (R2
= 0.26; P < 0.0001); and (3) while
species-area relationships were positive for both native and alien species, the non-linear
species-area relationship was much stronger and more predictable for native plant species.
In addition, we found a significant positive relationship between the mean gain in native
plant species from 100-m2
to 1000-m2
in the plots, to the mean gain in alien plant species
over the same spatial scales. Thus, alien species may be responding to similar factors responsible
for native species increases with area (e.g. habitat heterogeneity, disturbance,
water availability; Fig.3). Again, the polynomial model was a better fit than a linear model.
Regional-scale results
We found a positive relationship between cumulative native and alien species (in a given
vegetation type) across the 37 vegetation types in the survey (Fig. 4). Once more, the poly-
410 Preslia 78: 405­426, 2006
nomial model was a better fit than a linear model. Rare vegetation types such as aspen stands
in Colorado and perennial riparian types in Utah, and the northern mixed grass prairie type
in Montana exemplified native and alien species-rich habitats. Vegetation types with low cumulative
native species (e.g. tundra and pinyon-juniper) with increased sampling effort, usually
had high species composition overlap among plots, and thus lower beta-diversity in native
and alien species. Measured in this way, native beta-diversity in a vegetation type explained
33% of the variation in the beta-diversity of alien plant species (Fig. 4).
Stohlgren et al.: Scale and plant invasions 411
Table 1. ­ Correlations of mean native species cover per plot (averaged from all 1-m
2
subplots in each vegetation
type) and the richness of native and alien plant species at various spatial scales; n = 35 vegetation types with at
least four 1000-m
2
plots in each type (see Appendix 1).
Native species cover to: Slope Intercept R P
1-m
2
(native species richness) 0.086 2.057 0.595 0.0001
10-m
2
(native species richness) 0.149 3.914 0.657 0.0001
100-m
2
(native species richness) 0.229 7.137 0.711 0.0001
1000-m
2
(native species richness) 0.349 16.539 0.719 0.0001
1-m
2
(alien species richness) ­0.015 1.137 ­0.379 0.017
10-m
2
(alien species richness) ­0.016 1.460 ­0.270 0.096 (ns)
100-m
2
(alien species richness) ­0.020 2.221 ­0.241 0.139 (ns)
1000-m
2
(alien species richness) ­0.012 3.262 ­0.085 0.608 (ns)
-1
0
1
2
3
4
5
1 10 100 1000
y = 0.033x2
+ 0.102x ­ 0.028
R 2
= 0.132 n = 143
P < 0.0001
Plot area (m2)
Slopeofnativeto
speciesrichness
Tallgrass
Aspen CO
Spring
Fig. 2. ­ Relationship between the slope of correlations of native to alien species richness, averaged for each of the
37 vegetation types at 1-m
2
, 10-m
2
, 100-m
2
, and 1000-m
2
scales. The coefficients of variation on the slope were
1390%, 94%, 34%, and 25% for the 1-m
2
, 10-m
2
, 100-m
2
, and 1000-m
2
scales, respectively.
In support of biotic resistance arguments, we generally found significant negative relationships
between native species richness (or biomass) and the cover, biomass, relative
cover, and relative biomass of alien plant species (Fig. 5). For example, 26% of the variation
in the relative cover of alien species in a vegetation type could be explained by a negative
relationship with native species richness (Fig. 5d). Likewise, about 16% of the variation
in the cover of alien species per plot in a vegetation type could be explained by a nega-
412 Preslia 78: 405­426, 2006
0.0
1.0
2.0
3.0
4.0
5.0
6.0
0.0 5.0 10.0 15.0 20.0 25.0 30.0
y = 0.008x2 - 0.152x + 1.811
R 2 = 0.13 P < 0.05
Spring
Wet meadow, UT
Willow
Irrigated
Shortgrass
Steppe
Pinyon -
Juniper
Disturbed
Aspen, CO
Juniper
Mean native species gain (from 100m2 to 1000m2 )
Meanspeciesgain
(from100m2to1000m2)
Fig. 3. ­ Gain in native versus alien plant species from 100-m
2
plots to 1000-m
2
plots in 37 vegetation types in the
central Unites States, averaged by vegetation type.
0
5
10
15
20
25
30
35
40
45
50
0 100 200 300 400 500
y = 0.0002x 2
­ 0.0232x + 9.12
R2
= 0.33 P < 0.001
N. Mixed Grass,
Prairie, MT
Aspen, COIrrigated
Shortgrass
Steppe
Spruce - fir, CO
Desert
Mixed Grass
Cumulative native species
Cumulativespecies
Fig. 4. ­ The relationship of cumulative native and alien species by vegetation type (i.e. an estimate of native and
alien beta-diversity for a vegetation type) for the 37 vegetation types.
Stohlgren et al.: Scale and plant invasions 413
1.2 1.3 1.4 1.5 1.6 1.7
Native species richness
0.0
0.5
1.0
1.5
ccccoooovvvveeeerrrr
1.2 1.3 1.4 1.5 1.6 1.7
Native species richness
0
1
2
3
bb
bb
ii
ii
oo
oo
mm
mm
aa
aa
ss
ss
ss
ss
1.2 1.3 1.4 1.5 1.6 1.7
Native species richness
0.0
0.5
1.0
1.5
2.0
R
R
R
R
e
e
e
e
l
l
l
l
a
a
a
a
t
t
t
t
i
i
i
i
v
v
v
v
e
e
e
e
1.2 1.3 1.4 1.5 1.6 1.7
Native species richness
0.00
0.05
0.10
0.15
0.20
1 2 3 4 5
Native species biomass
0.0
0.5
1.0
1.5
1 2 3 4 5
Native species biomass
0
1
2
3
1 2 3 4 5
Native species biomass
0.0
0.5
1.0
1.5
2.0
1 2 3 4 5
Native species biomass
0.00
0.05
0.10
0.15
0.20
y = -2.65x + 4.62
R2 = 0.14 P = 0.012
y = -0.24x + 0.41
R2
= 0.26 P = 0.001
y = -0.11x + 0.62
R 2 = 0.02 P = 0.18
y = -1.36x + 1.92
R2 = 0.16 P = 0.008
y = -0.14x + 1.24
R2
= 0.001 P = 0.47
R2 = 0.04
P = 0.12
y = -0.22x + 1.70
y = -0.03x + 0.15
R2 = 0.10 P = 0.03
R2 = 0.26
P = 0.001
y = -2.46x + 4.57
a
g h
e f
dc
b
Fig. 5. ­ The relationships between native plant species richness (a­d) and biomass (e­h) to alien species cover,
biomass, relative cover, and relative biomass for 37 vegetation types. Data were log-transformed.
tive relationship with native species richness (Fig. 5a). The relationships of alien species
cover, biomass, relative cover, and relative biomass for the 37 vegetation types were
weaker for native biomass (as we calculated it; Fig. 5e-h) compared to native species richness
(Fig. 5a-d). There was considerable natural variation evident in all the graphs, and
three of the eight relationships were not significant (Fig. 5).
The cover, biomass, relative cover, and relative biomass of alien plant species were
strongly positively related to alien species richness per plot for the 37 vegetation types (Fig.
6). These relationships were far stronger and more predictable than the relationships to na-
414 Preslia 78: 405­426, 2006
Table 2. ­ The mean coefficient of variation of native and alien species richness and cover in 1-m
2
subplots (averaged
by vegetation type). The minimum and maximum of the mean coefficient of variation among vegetation
types are also presented.
Mean C.V. Min. Max.
Native species richness 5.3 0.52 0.3 0.8
Native species cover 38.1 0.85 0.4 1.4
Alien species richness 0.6 1.97 0.0 7.0
Alien species cover 3.9 3.36 0.0 12.1
0.0 0.2 0.4 0.6 0.8 1.0
species richness
species richness
species richness
species richness
0.0
0.5
1.0
1.5
s
s
s
s
p
p
p
p
e
e
e
e
c
c
c
c
i
i
i
i
e
e
e
e
s
s
s
s
ccoovveerr
0.0 0.2 0.4 0.6 0.8 1.0
0
1
2
3
b
b
i
i
o
o
m
m
a
a
s
s
s
s
0.0 0.2 0.4 0.6 0.8 1.0
0.0
0.5
1.0
1.5
2.0
R
R
e
e
l
l
a
a
t
t
i
i
v
v
e
e
0.0 0.2 0.4 0.6 0.8 1.0
0.00
0.05
0.10
0.15
0.20
y = 0.89x - 0.12
R2 = 0.57
P = 0.0001
y = 2.20x - 0.20
R2 = 0.58
P = 0.0001
y = 0.14x - 0.002
R2 = 0.43
P = 0.0001
y = 1.50x + 0.34
R2 = 0.52
P = 0.0001
a
c d
b
Fig. 6. ­The relationship of alien plant species richness to alien species cover, biomass, relative cover, and relative
biomass for 37 vegetation types. Data were log-transformed.
tive species richness per plot for the vegetation types (Fig. 5a­d). For example, 58% of the
variation in alien species biomass could be explained by a positive relationship with mean
alien species richness for a vegetation type (Fig. 6b). Likewise, 57% of the variation in alien
species cover could be explained by a positive relationship with alien species richness.
Habitat heterogeneity (i.e. the coefficient of variation in the richness or foliar cover of
native or alien plant species in 1-m2
subplots) varied greatly for native and alien species
(Table 2). For example, native species cover in 1-m2
subplots, with a coefficient of variation
of 85% of the mean was considerably more variable than native species richness per
Stohlgren et al.: Scale and plant invasions 415
0
0.4
0.8
1.2
1.6
0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8
y = 0.13x 3.84
R2 = 0.22
P < 0.05
0
0.2
0.4
0.6
0.8
1.0
1.2
y = 0.39x0.48
R2
= 0.04
P > 0.20
0
0.4
0.8
1.2
1.6
2.0
y = 0.24x3.50
R2 = 0.24
P < 0.05
Variation in native species cover
in 1 -m2 subplots (log10CV.)
RReellaattiivvee
speciesbiomassspeciescover
species
richness(1000-m2
)
Fig. 7. ­The relationship between the coefficient of variation of the foliar cover of native plants in 1-m2
subplots
in each vegetation type and alien species richness, relative cover, and relative biomass. Data were log-
transformed.
1-m2
(52%) in the same vegetation type. Meanwhile, the cover of alien species in 1-m2
subplots was about four times more variable than native species cover because only about
60% of the subplots contained alien species, and because that foliar cover was very
patchily distributed in some types (maximum CV over 1200%; Table 2).
We assessed whether the variation in native species cover in a plot might allow spatial
refugia for the establishment and dominance of alien plant species. We found no relationship
between alien plant species richness in 1000-m2
plots and variation of native foliar
cover. However, we found significant positive relationships between the coefficient of
variation of native cover and both the relative cover and relative biomass of alien plant species
for the 37 vegetation types (Fig. 7). Power models fit the data better than linear, exponential,
and polynomial models. The results suggested that the growth of alien plant species
was significantly greater in vegetation types with higher spatial variability in native
species cover (Fig. 7).
Discussion
We demonstrate how the scale of observation influences our understanding of the patterns
of invasion in many natural vegetation types. However, there are several caveats to observational
studies, and this study is no exception. We display statistical relationships between
native and alien species richness, cover, estimated biomass, and relative dominance
recognizing that cause and effect relationships cannot be determined by observational
studies. We also recognize that the sites used in this study were only measured once, and
they may not be representative of the regional vegetation types in space or time (Hamilton
et al. 2005, Pyšek & Hulme 2005, Pauchard & Shea 2006). The studies employed stratified
random sampling within major study areas (e.g. Rocky Mountain National Park, Grand
Staircase-Escalante National Monument, riparian and upland sites, etc.), but this was not
a stratified-random selection of plots or study sites throughout the region. Still, the data
represent a broad range of environmental conditions in the region ranging from desert
shrublands in Utah to tallgrass prairie in Minnesota, and from low-elevation grasslands to
forests and high-elevation tundra (Fig. 1, Appendix 1 and 2). When these regional data are
augmented with site-specific study results for natural vegetation types in California (Sax
2002, Keeley et al. 2003), Rhode Island (Bruno et al. 2004), and the southeast US (Brown
& Peet 2003), a more complete and consistent evaluation of scale and invasion emerges,
where invasion of alien plant species and coexistence with native plant species likely increase
with spatial scale (Stohlgren et al. 1999, Knight & Reich 2005).
We emphasized comparisons of native to alien species relationships across scales from
1 m2
to 1000 m2
(within plots). And, within a vegetation type, native species richness and
cover could vary considerably (Table 1, Appendix 2). On average across vegetation types,
alien species represent only 10% of the total foliar cover, and only 9% of the total species
richness per plot in a vegetation type. Only five vegetation types had > 10% cover of alien
species (irrigated shortgrass steppe, the wet meadow type in Utah, disturbed pinyon-juniper-sage,
the perennial riparian type, and the desert mixed-grass type; Appendix 2). Thus,
observed patterns may not represent other vegetation types or associations, or extremely
disturbed or highly invaded habitats, but they are corroborated in burned areas in California
(Keeley et al. 2003) and Utah (Evangelista et al. 2004).
416 Preslia 78: 405­426, 2006
We do not presume to distinguish among the many possible causes for the patterns we observed.
Evaluating the complex processes of escape from pathogens and predators, niche
sharing and overlap, quantifying seed dispersal (and longevity and viability in the soil), lifehistory
characteristics and many other potential causal factors are beyond the scope of this
investigation (Hamilton et al. 2005). We assume that the patterns we observed follow wellestablished
observations about natural ecosystems: (1) both native and alien species richness
generally increase with the area surveyed (Arrhenius 1921, Stohlgren et al. 1999); and (2)
environmental heterogeneity also increases with spatial scale (Palmer 1994, Jiang & Morin
2004, Davies et al. 2005), and this likely influences establishment and growth of alien species
where propagules are available (Table 1, Figs 2­4 and 7). Thus, it is likely that the rates
of immigration of native plant species and the invasion of alien species are heavily influenced
by a multitude of factors that co-vary with spatial and temporal scales such as climate
and weather, vegetation structure, micro- and macro-disturbances, resource availability, species
pools and propagule pressure, and associated ecosystem processes (e.g. herbivory, competition,
disease, hybridization, adaptation).
Effects of scale on the establishment of alien species
We were surprised to find that: (1) at the 1-m2
scale, about 60% of the vegetation types had
positive relationships between native and alien species richness; (2) only two vegetation
types maintained negative relationships between native and alien species richness as
scales increased to 1000 m2
; and (3) the mean slope of the relationship between native and
alien species increased significantly from the 1- to 1000-m2
scale (Fig. 2). However, these
findings provide possible mechanisms for previously reported patterns (Stohlgren et al.
1999, 2003) and perhaps observational studies in other vegetation types in California (Levine
2000, Keeley et al. 2003), Rhode Island (Bruno et al. 2004), and North Carolina
(Brown & Peet 2003, Fridley et al. 2004): positive relationships strengthen between native
and alien species richness at scales > 1-m2
. A statistical caveat is that at very small spatial
scales, the relationship between native and alien species may be affected by the sizes of individuals
(Fridley et al. 2004). So we tend to emphasize the more significant and positive
relationships between native and alien species richness at scales >100-m2
.
In the individual plant's extended neighbourhood (from 100 m2
to 1000 m2
in the same
habitat), it was clear that the average slope of the relationship between native and alien
species richness increased in a significant, non-linear pattern (Fig. 2), and that native and
alien species accumulation were positively associated (Fig. 3). It is well established that
species richness increases with area (Arrhenius 1921, Palmer 1994). In our study areas,
native plant species richness increased faster than alien plant species richness with plot
area. We propose that similar factors associated with native species increases with area,
such as habitat heterogeneity, extensions of environmental gradients, and increased probabilities
of encountering disturbed habitats or micro habitats, also are responsible for increasing
establishment of alien plant species as the spatial scale of observation is increased
(Stohlgren et al. 1999, 2001, 2002, 2003). Fewer species in the local and regional species
pools, time since invasion, and many other factors may have contributed to the less-steep
species-area relationship for alien plant species in the study areas.
It was intriguing to measure a weakening relationship between alien species richness
and native species foliar cover with increasing area, despite an increase in native species
Stohlgren et al.: Scale and plant invasions 417
richness with area and an increasing positive relationship between native species richness
and foliar cover per plot across vegetation types (Table 1). It must be that despite the increasing
number of native species in the extended plant neighbourhood, opportunities still
exist in many vegetation types for the increasing establishment of alien species. We suspect
that even modest changes in the spatial extent of the study (e.g. 1 m2
to 10 m2
, or 10 m2
to 100 m2
, etc.) may add considerably to local heterogeneity, niche availability, small-scale
disturbances, or resource availability related to plant mortality, herbivory, or loss of competition
prowess as a result of age, pathogens, climate, or many other factors that favour
co-existence (Table 2; also see Huston 2004, Levine et al. 2004).
A Theory of "Biotic Acceptance"
We speculate that early in the invasion of any area greater than 1 m2
(Figs. 2, 3), native species
greatly outnumbered newly arriving invaders, but that biotic resistance (Fig. 5) becomes
overwhelmed by "biotic acceptance" (Figs 2­4 and 6), where co-existence (Levine
et al. 2003, 2004) is a stronger force than competitive exclusion (Grime 1973, Corbin &
D'Antonio 2004), resulting in the broad-scale establishment of many alien species. The
theory of biotic acceptance would suggest that natural ecosystems tend to accommodate
the establishment and coexistence of introduced species despite the presence and abundance
of native species (Table 3). This is in sharp contrast to the previous framework of biotic
resistance, where competitive exclusion is the dominant mechanism determining the
structure and composition of communities. Our data strongly supported this theory of
biotic resistance across scales from meters to regions. Disturbance and increasing habitat
suitability for invasive species, along with a positive feedback cycle due to increased
propagule pressure (from growing "source" populations of invasive species) may further
facilitate the invasion process (Hobbs & Huenneke 1992, D'Antonio et al. 1999, Levine et
al. 2004, Pyšek & Hulme 2005).
What can we say about the potential of biotic acceptance in the establishment phase of
the invasion process? Based on these landscape- to regional-scale datasets, we would predict
that across the United States, the introduction and establishment of alien plant species
(i.e. biotic acceptance) would be greatest in areas high in native species richness and with
optimal conditions for plant growth. This is exactly the pattern observed at county, state,
region, and national scales (Brown & Peet 2003, Stohlgren et al. 2003, 2005a, 2006, Crosier
& Stohlgren 2004, Dark 2004). Strikingly similar results have been reported for South
Africa (Richardson et al. 2005).
These very broad-scale patterns might be predicted by a variety of conceptual models
(Shea & Chesson 2002, Huston 2004, Tilman 2004). However, only Huston's (2004) dynamic
equilibrium model fits our observations at the scales of plant neighbourhoods,
plots, vegetation types, regions, and the nation. The dynamic equilibrium model allows for
extrinsic factors and species diversity to increase across all spatial scales, productivity gradients,
and disturbance regimes within vegetation types or across regions.
Effects of scale on alien species dominance
For an alien plant species to attain dominance amongst well-established native plant species
remains a difficult task. The establishing alien species must compete in environments
where native species richness and cover are significantly positively related at 1-m2
scales
418 Preslia 78: 405­426, 2006
(R2
= 0.35; P< 0.0001), and where native species richness and estimated biomass are significantly
positively related at 1000-m2
scales across all vegetation types (R2
= 0.14; P <
0.0001). So, it was not surprising to see some local (plot-scale) evidence of biotic resistance.
However, many of the relationships between native and alien species richness,
cover, and biomass are weak (i.e. R2
values ranging from 0.001 to 0.36) with an average of
only 12% of the variation explained at the 1000-m2
scale (Fig. 5). Many other factors must
be important in determining invasion success in space and time (Stohlgren et al. 1999,
Bashkin et al. 2003, Huston 2004).
Availability of light, water, and nutrients may be important in invasion success (i.e. the
relative cover of alien plant species). While only five of the 37 vegetation types studied had
>10% relative cover of alien plant species, four of those vegetation types had higher water
availability relative to surrounding vegetation types: irrigated shortgrass steppe (alien relative
cover = 40%), wet meadow in Utah (35%) perennial riparian areas in Utah (17%),
and freshwater springs in Utah (16%). Likewise, the burned pinyon-juniper-sage type in
Utah had 15% relative cover of alien species perhaps reflecting greater light, water, and nitrogen/phosphorus
availability combined with decreased competition from native shrubs
and trees, which were consumed by the fire (Evangelista et al. 2004). Desert mixed grass
plots with 21% relative alien species cover typically have higher native species richness,
soil fertility, plant production, and corresponding higher levels of grazing than adjacent,
more xeric plant associations (e.g. blackbrush, desert shrub types; Bashkin et al. 2003, Appendix
1). Within the scale of a few hectares, we often have observed small nutrient-rich
sites serving as focal points of invasion (Stohlgren et al. 1997, 1998b, 1999, 2001).
There are several ways in which a alien species might become locally dominant in natural
landscapes. Local, infrequent disturbances such as fire (Fox & Fox 1986, Keeley et al.
2003) and flooding (DeFerrari & Naiman 1994) often have been proposed as prerequisites
for invasion success, but we believe more gradual and wide-spread invasions may be more
typical at landscape scales (Stohlgren et al. 1997, 1999), regional scales (Stohlgren et al.
2002), and national scales as alien species establish and reproduce in favourable climates,
Stohlgren et al.: Scale and plant invasions 419
Table 3. ­ General comparison of the theories of biotic resistance and biotic acceptance.
Biotic Resistance Biotic Acceptance
Definition "Forces of nature", natural processes or
ecosystem properties that contribute to
a reduction in the rate of establishment and
spread of introduced species. [paraphrasing
Elton 1958 by D'Antonio & Thomsen 2004]
Where natural ecosystems tend to
accommodate the establishment and
coexistence of introduced species despite the
presence and abundance of native species.
[This paper]
Proposed
mechanisms
Competitive exclusion, predation, herbivory,
pathogens, among others.
Individual and species turnover in space and
time, habitat heterogeneity, disturbance, open
niches, and dispersal, among others.
Primary
assumptions
Assumes neighbourhood interactions scale
directly to large areas and determine
community structure and composition.
Assumes environmental heterogeneity,
environmental gradients, disturbance and
turnover increase with spatial scale.
on fertile soils, and in conjunction with other factors that also contribute to high native species
diversity (Stohlgren et al. 2003, 2005a, b, 2006).
The strong relationships between alien species richness and alien cover or biomass may
be cause for concern (Fig. 6). These field data (Figs 4 and 6), and continental-scale findings
(Stohlgren et al. 2003, 2005a, 2006) strongly suggest that the continued establishment
of alien plants may be directly linked to the factors responsible for growth, cover, and
biomass of other alien plants in the wide range of vegetation types studied (Fig. 6). Withinplot
habitat heterogeneity (Fig. 7, Davies et al. 2005) combined with high resource availability
(e.g. energy/water/nutrients; Bashkin et al. 2003, Stohlgren et al. 2005b) and disturbance
(Fox & Fox 1986) may promote the coexistence of native and alien species (Fig.
4). However, we are also learning that habitat heterogeneity around plots (~240 m diameter)
may also contribute to coexistence (Kumar et al. 2006). It is too early to tell if there
will be widespread dominance of alien species as is evident in the lowlands in Hawaii
(Mack et al. 2000), the foothills of California (Keeley et al. 2003), and some riparian zones
in the United States (DeFerrari & Naiman 1994, Stohlgren et al. 1998b).
Acknowledgements
Funding for the vegetation sampling in Colorado was provided by the U.S. Geological Survey, while the funding
for sampling in the Grand Staircase-Escalante National Monument, Utah, was provided by the Bureau of Land
Management. This work would have been impossible without the enthusiastic services of over 30 research assistants,
graduate students, and volunteers. We received logistic support from the staffs of Rocky Mountain National
Park, Grand Staircase-Escalante National Monument, the USGS Fort Collins Science Center, and the Natural Resource
Ecology Laboratory at Colorado State University. Other studies used in the synthesis were either funded or
supported by the USDA Forest Service, the National Biological Survey (Service), the National Park Service, and
the Environmental Protection Agency. Current funding for synthesis and analysis was obtained from NASA and
the U.S. Geological Survey. Alycia Crall and anonymous reviewers provided very helpful comments to earlier
versions of the manuscript. To all we are grateful.
Souhrn
V práci je analyzován vztah mezi druhovou bohatostí, pokryvností a odhadnutoubiomasou původních a nepůvodních
druhů v různém prostorovém měřítku. Datový soubor zahrnoval 7051 ploch velikosti 1 m2
, 1443 velikosti
10 m2
a 727 velikosti 100 m2
, vřazených do 727 1000 m2
velkých ploch, rozmístěných v 37 typech přirozené vegetace
sedmi států centrální části USA. Druhová bohatost původních a nepůvodních druhů (vyjádřená jako průměr
pro všechny vegetační typy) průkazně rostla s velikostí plochy. Se zvětšujícím se měřítkem byl vztah mezi oběma
proměnnými průkaznější a vzrůstala četnost pozitivních vztahů (u ploch velikosti 1000 m2
byl nalezen pozitivní
vztah v 80 % případů). Jak původní, tak nepůvodní druhy pravděpodobně reagují na dostupnost zdrojů, jež narůstá
s měřítkem studia, a stanovištní heterogenitu, jež se zvětšuje se stoupající velikostí plochy. Byl nalezen průkazný
pozitivní vztah mezi stanovištní heterogenitou vegetačního typu, vyjádřenou jako hodnota variačního koeficientu
pokryvnosti původních druhů v 1 m2
plochách, a relativní pokryvností a relativní biomasou nepůvodních
druhů. Pro měřítko 1000 m2
byl zjištěn slabý negativní vztah mezi bohatostí původních druhů a bohatostí, pokryvností,
biomasou a relativní pokryvností nepůvodních druhů, ale velmi silný pozitivní vztah mezi bohatostí
nepůvodních druhů a jejich pokryvností, relativní pokryvností a relativní biomasou. Tyto výsledky, podpořené
mnoha dalšími studiemi v přirozené vegetaci, podporují teorii ,,biotické akceptance", podle níž do přirozených
ekosystémů pronikají nepůvodní druhy bez ohledu na přítomnost původních druhů a jejich abundanci.
420 Preslia 78: 405­426, 2006
References
Arrhenius O. (1921): Species and area. ­ J. Ecol. 9: 95­99.
Bashkin M., Stohlgren T. J., Otsuki Y., Lee M., Evangelista P. & Belnap J. (2003): Soil characteristics and plant
exotic species invasions in the Grand Staircase-Escalante National Monument, Utah, USA. ­ Appl. Soil Ecol.
22: 67­77.
Brown R. L. & Peet R. K. (2003): Diversity and invasibility of southern Appalachian plant communities. ­ Ecology
84: 32­39.
Bruno J. F., Kennedy C. W., Rand T. A. & Grant M. B. (2004): Landscape-scale patterns of biological invasions in
shoreline plant communities. ­ Oikos 107: 531­540.
Case T. J. (1990) Invasion resistance arises in strongly interacting species-rich model competition communities. Proc.
Natl. Acad. Sci. USA 87: 9610­9614.
Chong G. W. (2002): Multi-scale sampling of native and non-native plant diversity: examples of data analyses and
applications. ­ Thesis, Colorado State University, Fort Collins.
Chytrý M., Pyšek P., Tichý L., Knollová I. & Danihelka J. (2005): Invasions by alien plants in the Czech Republic:
a quantitative assessment. ­ Preslia 77: 339­354.
Comstock J. P. & Elhleringer J. R. (1992): Plant adaptation in the Great Basin and Colorado Plateau. ­ Great Basin
Natur. 52: 195­215.
Corbin J. D. & D'Antonio C. M. (2004) Competition between native perennial and exotic annual grasses: Implications
for an historical invasion. ­ Ecology 85: 1273­1283.
Crosier C.S. & Stohlgren T. J. (2004): Improving biodiversity knowledge with data set synergy: A case study of
nonnative plants in Colorado. ­ Weed Technol. 18: 1441­1444.
D'Antonio C. M., Dudley T. L. & Mack M. (1999): Disturbance and biological invasions: direct effects and feedbacks.
­ In: Walker L. R. (ed.), Ecosystems of disturbed ground, p. 413­452,Elsevier, New York.
D'Antonio C. M. & Thomsen M. (2004): Ecological resistance in theory and practice. ­ Weed Technol. 18:
572­1577.
Dark S. J. (2004): The biogeography of invasive alien plants in California: an application of GIS and spatial regression
analysis. ­ Diversity Distrib. 10: 1­9.
Davies K. E., Chesson P., Harrison S., Inouye B. D., Melbourne B. A. & Rice K. J. (2005): Spatial heterogeneity
explains the scale dependence of the native-exotic diversity relationship. ­ Ecology 86: 1602­1610.
DeFerrari C. M. & Naiman R. J. (1994): A multi-scale assessment of the occurrence of exotic plants on the Olympic
Peninsula, Washington. ­ J. Veget. Sci. 5: 247­258.
Elton C. S. (1958): The ecology of invasions by animals and plants. ­ Methuen, London.
Evangelista P., Stohlgren T. J., Guenther D. & Stewart S. (2004): Vegetation response to fire and postburn seeding
treatments in juniper woodlands of the Grand Staircase-Escalante National Monument, Utah. ­ Western
North Amer. Natur. 64: 293­305.
Fox M. D. & Fox B. J. (1986): The susceptibility of natural communities to invasion. ­ In: Groves R. H. & Burdon
J. J. (eds.), Ecology of biological invasions: An Australian perspective, p. 57­66, Cambridge Univ. Press,
Cambridge.
Fridley J. D., Brown R. L. & Bruno J. E. (2004): Null models of exotic invasion and scale-dependent patterns of
native and exotic species richness. ­ Ecology 85: 3215­3222.
Fridley J. D., Stachowicz J. J., Naeem S., Sax D. F., Seabloom E. W., Smith M. D., Stohlgren T. J., Tilman D. &
Von Holle B. (2006): The invasion paradox: reconciling pattern and process in species invasions. ­ Ecology
(in press).
Grime J. P. (1973): Competitive exclusion in herbaceous vegetation. ­ Nature 242: 344­347.
Hamilton M. A., Murray B. R., Cadotte M. W., Hose G. C., Baker A. C., Harris C. J. & Licari D. (2005): Life-history
correlates of plant invasiveness at regional and continental scales. ­ Ecol. Lett. 8: 1066­1074.
Hobbs R. J. & Huenneke L. F. (1992): Disturbance, diversity, and invasion: implications for conservation. Conserv.
Biol. 6: 324­337.
Hubbell S. P. (2001): The unified neutral theory of biodiversity and biogeography. ­ Princeton Univ. Press,
Princeton.
Huston M. A. (1997): Hidden treatments in ecological experiments: re-evaluating the ecosystem function of
biodiversity. ­ Oecologia 110: 449­460
Huston M. A. (2004): Management strategies for plant invasions: manipulating productivity, disturbance, and
competition. ­ Diversity Distrib. 10: 167­178.
Jiang L. & Morin P. J. (2004): Productivity gradients cause positive diversity-invasibility relationships in microbial
communities. ­ Ecol. Lett. 7: 1047­1057.
Stohlgren et al.: Scale and plant invasions 421
Keeley J. E., Lubin D. & Fotheringham C. J. (2003) Fire and grazing impacts on plant diversity and alien plant invasions
in the southern Sierra Nevada. ­ Ecol. Appl. 13: 1355­1374.
Kennedy T. A., Naeem S., Howe K. M., Knops J. M. H., Tilman D. & Reich P. (2002): Biodiversity as a barrier to
ecological invasion. ­ Nature 417: 636­638.
Knight K. S. & Reich P. B. (2005): Opposite relationships between invasibility and native species richness at
patch versus landscape scales. ­ Oikos 109: 81­88.
Knops J. M. H., Tilman D., Naeem S. & Howe K. M. (1997): Biodiversity and plant invasions in experimental
grassland plots. ­ Bull. Ecol. Soc. Amer. 18: 125.
Kumar S., Stohlgren T. J. & Chong G.W. (2006): Effects of spatial heterogeneity on native and non-native plant
species richness. ­ Ecology (in press).
Lee M. (2001): Non-native plant invasions in Rocky Mountain National Park: Linking species traits and habitat
characteristics. ­ Thesis, Colorado State University, Fort Collins.
Levine J. M. (2000): Species diversity and biological invasions: relating local process to community pattern. Science
288: 852­854.
Levine J. M., Adler P. B. & Yelenik S. G. (2004): A meta-analysis of biotic resistance to exotic plant invasions. Ecol.
Lett. 7: 975­989.
Levine J. M., Vila M., D'Antonio C. M., Dukes J. S., Grigulis K. & Lavorel S. (2003): Mechanisms underlying
the impacts of exotic plant invasions. ­ Proc. R. Soc. London B 270: 775­781.
Mack R. N., Simberloff D., Lonsdale M., Evans H., Clout M. & Bazzaz F. (2000): Biotic invasions: causes, epidemiology,
global consequences and control. ­ Issues in Ecology 5: 1­20.
Palmer M. W. (1994): Variation in species richness: toward a unification of hypotheses. ­ Folia Geobot. Phytotax.
29: 511­530.
Pauchard A. & Shea K. (2006): Integrating the study of non-native plant invasions across spatial scales. ­ Biol.
Invas. 8: 399­413.
Pyšek P. & Hulme P. E. (2005): Spatio-temporal dynamics of plant invasions: Linking pattern to process. Ecoscience
12: 302­315.
Rejmánek M. (1996): Species richness and resistance to invasions. ­ In: Orians H., Dirzo R. & Cushman J. H.
(eds.), Biodiversity and ecosystem processes in tropical forests, Ecological Studies 122, p. 153­172,
Springer-Verlag, Berlin.
Richardson D. M. & Pyšek P. (2006): Plant invasions: merging the concepts of species invasiveness and community
invasibility. ­ Progr. Phys. Geogr. 30: 409­431.
Richardson D. M., Rouget M., Ralston S. J., Cowling R. M., Van Rensburg B. J. & Thuiller W. (2005): Species
richness of alien plants in South Africa: Environmental correlates and the relationship with indigenous plant
species richness. ­ Ecoscience 12: 391­205.
Sax D. F. (2002): Native and naturalized plant diversity are positively correlated in scrub communities of California
and Chile. ­ Diversity Distrib. 8: 193­210.
Shea K. & Chesson P. (2002): Community ecology theory as a framework for biological invasions. ­ Trends Ecol.
Evolut. 17: 170­176.
Shultz L. M. (1998): The flora and fauna of the Colorado Plateau: What do we know? ­ In: Hill L. M. (ed.), Learning
from the land, Grand Staircase-Escalante National Monument Science Symposium, p. 203­210, Paragon
Press, Salt Lake City.
Stohlgren T. J., Barnett D., Flather C., Fuller P., Peterjohn B., Kartesz J. & Master L. L. (2006): Species richness
and patterns of invasion in plants, birds, and fishes in the United States. ­ Biol. Invas. 8: 427­447.
Stohlgren T. J., Barnett D. T. & Kartesz J. (2003): The rich get richer: patterns of plant invasions in the United
States. ­ Front. Ecol. Environ. 1: 11­14.
Stohlgren T. J., Barnett D. T., Flather C., Kartesz J. & Peterjohn B. (2005a): Plant species invasions along the latitudinal
gradient in the United States. ­ Ecology 86: 2298­2309
Stohlgren T. J., Binkley D., Chong G. W., Kalkhan M. A., Schell L. D., Bull K. A., Otsuki Y., Newman G.,
Bashkin M. & Son Y. (1999): Exotic plant species invade hot spots of native plant diversity. ­ Ecol. Monogr.
69: 25­46.
Stohlgren T. J., Bull K. A. & Otsuki Y. (1998a): Comparison of rangeland vegetation sampling techniques in the
Central Grasslands. ­ J. Range Manage. 51: 164­172.
Stohlgren T. J., Bull K. A., Otsuki Y., Villa C. A. & Lee M. (1998b): Riparian zones as havens for exotic plant species.
­ Plant Ecol. 138: 113­125.
Stohlgren T. J., Chong G. W., Kalkhan M. A. & Schell L. D. (1997): Rapid assessment of plant diversity patterns:
a methodology for landscapes. ­ Environ. Monitor. Assessm. 48: 25­43.
422 Preslia 78: 405­426, 2006
Stohlgren T. J., Chong G. W., Schell L. D., Rimar K. A., Otsuki Y., Lee M., Kalkhan M. A. & Villa C. A. (2002):
Assessing vulnerability to invasion by nonnative plant species at multiple spatial scales. ­ Environ. Manage.
29: 566­577.
Stohlgren T. J., Falkner M. B. & Schell L. D. (1995): A modified-Whittaker nested vegetation sampling method. Vegetatio
117: 113­121.
Stohlgren T. J., Guenther D. A., Evangelista P. H. & Alley N. (2005b): Patterns of plant species richness, rarity,
endemism, and uniqueness in an arid landscape. ­ Ecol. Appl. 15: 715­725.
Stohlgren T. J., Otsuki Y., Villa C.A., Lee M. & Belnap J. (2001): Patterns of plant invasions: a case example in
native species hotspots and rare habitats. ­ Biol. Invas. 3: 37­50.
Tilman D. (1997): Community invasibility, recruitment limitation, and grassland biodiversity. ­ Ecology 78:
81­92.
Tilman D. (2004): Niche tradeoffs, neutrality, and community structure: A stochastic theory of resource competition,
invasion, and community assembly. ­ Proc. Natl. Acad. Sci. USA 101: 10854­10861.
Waters M. A. (2003): Species richness, vegetation cover, and disturbance relationships in an arid ecosystem. Thesis,
Colorado State University, Fort Collins.
Received 18 May 2006
Revision received 17 August 2006
Accepted 31 August 2006
Appendix 1. ­ Vegetation types and codes (i.e. short names) identified in this and previous studies (Stohlgren et
al. 1998b, 1999, 2001, 2002), site descriptions, locations, and number of 1000 m
2
sample plots (n).
Vegetation type
code
Description and location n
Aspen Populus tremuloides stands in Grand Staircase-Escalante National Monument, UT 6
AspenCO Populus tremuloides stands in the Colorado Rocky Mountains 45
AspenOldCO Decadent Populus tremuloides stands in Arapaho-Roosevelt National Forest, CO 5
Blackbrush Coleogyne ramosissima dominated stands in Grand Staircase-Escalante National
Monument, UT
27
CushMG Cushion plant communities and mixed grass prairie dominated areas in Northern
WY
8
Desert Shrub Ephedra spp., Gutierrezia sarothrae, Atriplex confertifolia, Ceratoides lanata
and Chrysothamnus spp. dominated stands in Grand Staircase-Escalante National
Monument, UT
29
DesertMG Desert Mixed Grass prairie of Badlands National Park, SD 8
DesertShGr Desert shrub species mixed with Stipa spp., Hilaria jamesii, Agropyron smithii,
Bouteloua gracilis, and Bromus tectorum in Grand Staircase-Escalante National
Monument, UT
16
Douglas fir Psuedotsuga menziesii stands in Northern CO Rocky Mountains 10
Dry meadow Carex helianthus and Artemisia tridentata dominated meadows in Rocky Mountain
National Park, CO
9
Juniper Juniperus osteosperma stands in Grand Staircase-Escalante National Monument,
UT
37
Lodgepole Pinus contorta stands in Rocky Mountain National Park, CO 23
MixGrPrWyo Mixed grass prairie of Bouteloua gracilis, Koeleria pyramidata, Stipa comata,
and Artemisia frigida in Southeastern WY
4
Stohlgren et al.: Scale and plant invasions 423
NMixGrPrMT Northern mixed grass prairie dominated by Poa pratensis, Stipa comata,
Bromus japonicus, and Agropyron smithii in north-eastern WY, eastern MT, and
western SD
57
PerenRipUT Populus fremontii, Tamarix spp., Salix spp., and Elaeagnus angustifolia stands
in Grand Staircase-Escalante National Monument, UT
22
Pinyon Pine Pinus edulis stands in Grand Staircase-Escalante National Monument, UT 6
Pinyon-Junip P. edulus / Juniperus osteosperma mixed stands in Grand Staircase-Escalante
National Monument, UT
114
PJManz P. edulis / J. osteosperma /Arctostaphylos patula mixed stands in Grand Staircase-Escalante
National Monument, UT
6
PJOak P. edulis / J. osteosperma / Quercus spp. mixed stands in Grand StaircaseEscalante
National Monument, UT
18
PJSageDist Post-fire of P. edulis / J. osteosperma / Artemisia tridentata stands in Grand
Staircase-Escalante National Monument, UT, samples a few years after burning.
28
PondPineCO Pinus ponderosa stands in Northern CO Rocky Mountains 32
PondPineUT Pinus ponderosa stands in Grand Staircase-Escalante National Monument, UT 7
Rabbitbrush Chrysothamnus nauseosus dominated stands in Grand Staircase-Escalante National
Monument, UT
9
SageBrCO Artemesia tridentata dominated areas in western CO and southwestern WY 33
SageBrUT A. tridentata stands in Grand Staircase-Escalante National Monument, UT 37
MntShrubUT Cercocarpus montanus, Purshia mexicana, Amelanchier spp., and
Symphoricarpos spp. dominated overstory in Grand Staircase-Escalante National
Monument, UT
12
ShoGRStCUp Bouteloua gracilis and Opuntia spp. dominated Short grass steppe in Eastern CO 8
ShortGRStIrr Bromus inermis, Juncus balticus, Mulenbergia asperifolia, and Hordeum
jubatum dominated area in the San Luis Valley, CO
8
Spring Scirpus and Juncus spp. dominated stands in Grand Staircase-Escalante National
Monument, UT
2
Spruce Fir Picea engelmannii / Abies lasiocarpa stands in Rocky Mountain National Park, CO 11
Subalpine Pinus flexilis and A. lasiocarpa stands in Rocky Mountain National Park, CO 17
tallgrass pr Bromus inermis, Aster oblongifolia, and Symphoricarpos occidentalis dominated
tallgrass prairie at Pipestone National Monument, Minnesota
4
Tundra High elevation alpine tundra in Rocky Mountain National Park, CO 36
WetMeadCO Poa palustris, P. interior and Deschampsia caespitosa dominated meadows in
Rocky Mountain National Park, CO
12
WetMeadUT Juncus, Carex and Poa spp. mixed meadows in Grand Staircase-Escalante National
Monument, UT
3
wetMeadYELL Festuca idahoensis and Artemisia tridentata dominated wet meadows in Yellowstone
National Park, WY
9
Willow Salix spp. dominated stands in Rocky Mountain National Park, CO 9
424 Preslia 78: 405­426, 2006
Appendix 2. ­ Mean native (nat) and alien (ali) plant species richness (rich) and cover (cov) at the 1-m
2
scale, and
mean native and alien plant species richness at the 10-m
2
, 100-m
2
, and 1000-m
2
scale, respectively, by vegetation
type. Standard errors (SE) on second row of each vegetation type.
n nat rich
1 m
2
ali rich
1 m
2
nat cov
%
ali cov
%
nat rich
10 m
2
ali rich
10 m
2
nat rich
100 m
2
ali rich
100 m
2
nat rich
1000 m
2
ali rich
1000 m
2
Aspen 60 4.4 0.9 52.8 8.0 7.7 1.1 16.3 2.8 31.7 4.7
SE 0.2 0.1 4.6 2.1 0.6 0.1 1.4 0.7 3.2 1.0
AspenCO 448 9.2 0.4 88.6 2.5 16.5 0.8 27.4 1.4 46.7 3.7
SE 0.2 0.0 2.6 0.3 0.6 0.2 1.1 0.3 1.7 0.6
AspenOldCO 50 7.0 0.0 71.6 0.0 15.1 0.0 19.4 0.0 44.6 0.4
SE 0.6 0.0 6.1 0.0 3.2 0.0 4.1 0.0 4.4 0.2
Blackbrush 253 3.8 0.6 26.7 2.6 6.3 0.7 11.2 0.9 20.4 1.2
SE 0.1 0.0 1.4 0.4 0.3 0.1 0.9 0.2 1.1 0.2
CushMG 80 4.6 0.9 26.2 7.1 8.5 1.3 14.9 3.5 24.8 4.5
SE 0.2 0.1 2.9 1.6 1.0 0.4 1.2 1.2 3.1 1.6
Desert Shrub 270 3.9 0.7 13.0 1.8 7.5 0.9 11.2 1.3 21.6 1.9
SE 0.1 0.0 0.9 0.3 0.5 0.1 1.0 0.2 1.5 0.2
DesertMG 80 5.4 1.9 29.4 10.9 8.6 2.6 13.9 4.1 26.6 7.6
SE 0.2 0.2 2.3 2.3 1.0 0.4 1.9 0.8 2.8 0.8
DesertShGr 157 5.1 0.8 20.0 2.3 8.9 1.1 12.8 1.1 25.2 1.6
SE 0.2 0.1 1.6 0.3 0.5 0.1 1.2 0.2 1.7 0.2
Douglas fir 100 5.7 0.0 49.9 0.0 10.3 0.2 18.9 0.1 37.4 1.0
SE 0.5 0.0 4.3 0.0 1.7 0.1 3.0 0.1 6.2 0.4
Dry meadow 90 9.0 0.7 38.6 2.2 15.8 0.9 25.2 1.6 39.4 2.9
SE 0.4 0.1 1.7 0.4 1.2 0.2 2.9 0.3 3.4 0.6
Juniper 350 3.9 0.6 18.2 3.5 7.1 0.8 11.9 1.2 24.0 1.8
SE 0.1 0.0 1.3 0.5 0.4 0.1 0.9 0.2 1.4 0.2
Lodgepole 195 2.9 0.1 29.1 0.4 6.3 0.1 11.7 0.2 22.9 0.8
SE 0.1 0.0 2.2 0.4 0.5 0.0 1.2 0.1 1.9 0.2
MixGrPrWyo 40 9.3 0.1 40.9 0.0 14.5 0.5 21.3 0.5 29.3 2.5
SE 0.4 0.1 3.3 0.0 2.0 0.4 3.1 0.3 2.5 1.3
NMixGrPrMT 481 5.7 0.8 26.7 4.0 9.5 1.2 15.8 2.2 27.1 4.4
SE 0.2 0.1 1.0 0.4 0.6 0.1 1.0 0.3 1.4 0.4
PerenRipUT 193 3.0 1.1 32.6 12.3 5.7 2.0 10.6 2.9 24.5 5.8
SE 0.1 0.1 2.6 1.6 0.5 0.2 1.1 0.3 2.1 0.4
Pinyon Pine 59 3.2 0.3 31.2 0.9 5.5 0.3 12.0 0.5 23.7 0.8
SE 0.2 0.1 4.7 0.3 0.8 0.1 1.1 0.3 2.6 0.4
Pinyon-Junip 1064 3.3 0.3 25.6 1.4 6.2 0.4 11.2 0.6 23.2 1.1
SE 0.1 0.0 0.9 0.2 0.2 0.0 0.4 0.1 0.7 0.1
PJManz 60 4.8 0.1 33.3 0.1 7.3 0.1 18.7 0.2 32.7 0.3
SE 0.3 0.0 3.8 0.0 1.1 0.1 1.6 0.2 2.0 0.2
PJOak 175 4.1 0.2 41.6 0.4 8.4 0.3 14.7 0.3 30.2 1.2
SE 0.2 0.0 2.9 0.1 0.7 0.1 1.1 0.1 1.9 0.4
PJSageDist 280 2.8 1.8 12.8 12.6 5.2 2.4 9.2 3.2 16.7 3.8
SE 0.1 0.1 1.1 0.9 0.5 0.2 0.9 0.3 1.4 0.4
PondPineCO 296 5.5 0.2 37.0 0.5 12.5 0.5 21.0 0.7 34.3 1.9
SE 0.2 0.0 2.1 0.1 1.1 0.1 1.4 0.2 1.9 0.3
PondPineUT 68 3.5 0.2 37.6 0.9 6.9 0.3 13.3 0.6 26.3 0.6
SE 0.3 0.1 4.6 0.5 0.8 0.1 1.7 0.2 2.3 0.2
Rabbitbrush 89 2.4 0.6 17.5 4.7 5.3 0.7 10.2 1.3 23.0 3.0
SE 0.2 0.1 2.9 1.6 0.7 0.2 1.3 0.3 1.5 0.6
SageBrCO 327 5.3 0.7 29.9 3.4 10.2 1.0 14.7 1.5 25.5 2.4
SE 0.2 0.0 1.3 0.3 0.7 0.1 1.3 0.2 2.4 0.3
SageBrUT 368 3.7 0.6 25.4 3.2 6.2 0.8 9.4 1.0 20.0 1.6
SE 0.1 0.0 1.3 0.4 0.4 0.1 0.9 0.2 1.4 0.2
MntShrubUT 112 2.8 0.2 20.3 0.6 5.1 0.2 8.8 0.5 18.9 1.6
Stohlgren et al.: Scale and plant invasions 425
n nat rich
1 m
2
ali rich
1 m
2
nat cov
%
ali cov
%
nat rich
10 m
2
ali rich
10 m
2
nat rich
100 m
2
ali rich
100 m
2
nat rich
1000 m
2
ali rich
1000 m
2
SE 0.2 0.0 2.3 0.3 0.4 0.1 1.2 0.2 1.4 0.5
ShoGRStCUp 80 5.8 0.0 34.8 0.0 10.4 0.1 17.4 0.9 37.9 0.9
SE 0.3 0.0 2.4 0.0 0.7 0.1 2.4 0.5 5.1 0.4
ShortGRStIrr 80 4.3 2.9 34.1 32.2 7.4 5.2 12.0 6.9 20.0 10.0
SE 0.2 0.3 2.5 3.6 0.7 0.9 1.5 1.5 1.3 2.0
Spring 18 1.8 0.2 31.4 5.5 5.0 0.3 14.0 1.5 38.5 6.5
SE 0.3 0.1 8.1 3.8 0.6 0.3 1.0 0.5 3.5 2.5
Spruce Fir 101 6.2 0.1 65.8 0.1 11.1 0.2 20.2 0.3 33.5 0.5
SE 0.4 0.0 4.8 0.1 1.4 0.1 3.4 0.2 5.9 0.2
Subalpine 163 4.0 0.1 48.8 0.6 10.7 0.2 16.4 0.4 27.9 0.9
SE 0.2 0.0 3.1 0.3 1.2 0.1 2.1 0.2 2.6 0.3
Tallgrass pr 40 7.7 0.2 47.0 0.6 11.6 0.8 18.3 1.5 29.3 3.3
SE 0.5 0.1 4.8 0.4 1.9 0.4 3.0 0.6 2.8 0.9
Tundra 359 13.9 0.0 54.4 0.0 20.6 0.0 28.3 0.0 38.3 0.1
SE 0.2 0.0 1.0 0.0 0.6 0.0 1.1 0.0 1.6 0.0
WetMeadCO 120 7.3 0.4 66.4 4.2 11.8 0.7 19.5 1.4 35.6 3.8
SE 0.3 0.1 2.9 1.0 0.9 0.2 1.4 0.4 3.3 0.8
WetMeadUT 30 4.6 1.1 34.1 13.0 7.7 1.0 10.0 2.3 31.0 6.7
SE 0.4 0.2 4.8 3.7 2.2 0.3 2.5 0.9 5.6 0.9
WetMeadYELL 88 7.6 0.1 43.8 0.1 13.6 0.3 15.1 0.7 31.7 1.3
SE 0.3 0.0 3.1 0.1 0.5 0.1 1.3 0.3 2.4 0.4
Willow 90 7.3 0.3 58.4 0.6 12.0 0.6 23.0 1.4 41.3 4.2
SE 0.3 0.1 3.7 0.3 1.1 0.3 1.8 0.7 4.6 1.0
426 Preslia 78: 405­426, 2006