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Ecological Applications, 17(3), 2007, pp. 922–933
Ó 2007 by the Ecological Society of America
ABIOTIC CONSTRAINTS ECLIPSE BIOTIC RESISTANCE IN DETERMINING
INVASIBILITY ALONG EXPERIMENTAL VERNAL POOL GRADIENTS
FRITZ GERHARDT1,3
AND
SHARON K. COLLINGE1,2
1
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309 USA
2
Environmental Studies Program, University of Colorado, Boulder, Colorado 80309 USA
Abstract. Effective management of invasive species requires that we understand the
mechanisms determining community invasibility. Successful invaders must tolerate abiotic
conditions and overcome resistance from native species in invaded habitats. Biotic resistance
to invasions may reflect the diversity, abundance, or identity of species in a community. Few
studies, however, have examined the relative importance of abiotic and biotic factors
determining community invasibility. In a greenhouse experiment, we simulated the abiotic and
biotic gradients typically found in vernal pools to better understand their impacts on
invasibility. Specifically, we invaded plant communities differing in richness, identity, and
abundance of native plants (the ‘‘plant neighborhood’’) and depth of inundation to measure
their effects on growth, reproduction, and survival of five exotic plant species.
Inundation reduced growth, reproduction, and survival of the five exotic species more than
did plant neighborhood. Inundation reduced survival of three species and growth and
reproduction of all five species. Neighboring plants reduced growth and reproduction of three
species but generally did not affect survival. Brassica rapa, Centaurea solstitialis, and Vicia
villosa all suffered high mortality due to inundation but were generally unaffected by
neighboring plants. In contrast, Hordeum marinum and Lolium multiflorum, whose survival
was unaffected by inundation, were more impacted by neighboring plants. However, the four
measures describing plant neighborhood differed in their effects. Neighbor abundance
impacted growth and reproduction more than did neighbor richness or identity, with growth
and reproduction generally decreasing with increasing density and mass of neighbors.
Collectively, these results suggest that abiotic constraints play the dominant role in
determining invasibility along vernal pool and similar gradients. By reducing survival, abiotic
constraints allow only species with the appropriate morphological and physiological traits to
invade. In contrast, biotic resistance reduces invasibility only in more benign environments
and is best predicted by the abundance, rather than diversity, of neighbors. These results
suggest that stressful environments are not likely to be invaded by most exotic species.
However, species, such as H. marinum, that are able to invade these habitats require careful
management, especially since these environments often harbor rare species and communities.
Key words: abiotic constraints; biotic resistance; competition; diversity; environmental gradient; exotic
species; inundation; invasibility; vernal pools.
INTRODUCTION
Successful management of biological invasions requires that scientists, managers, and policymakers
understand why some communities are more vulnerable
to invasions than others. Ecologists have long debated
the relative importance of abiotic and biotic mechanisms
in determining community invasibility. Abiotic constraints hypotheses propose that exotic species are
unable to tolerate the abiotic conditions found in less
invaded communities (Fox and Fox 1986, Rejmánek
1989). In contrast, biotic resistance hypotheses propose
Manuscript received 29 June 2005; revised 24 July 2006;
accepted 31 August 2006. Corresponding Editor: D. D.
Breshears.
3 Present address: NorthWoods Stewardship Center, P.O.
Box 220, East Charleston, Vermont 05833 USA.
E-mail: [email protected]
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that interactions with native biota (e.g., competitors or
predators) exclude exotic species from less invaded
communities (Elton 1958, Fox and Fox 1986, Crawley
1987, Rejmánek 1989, Ewel et al. 1999, Mack et al.
2000). Despite numerous theoretical and empirical
studies, there is still no clear understanding of why
some communities are more vulnerable to invasions
than others.
Abiotic constraints allow only species with appropriate morphological and physiological traits to invade.
Few studies, however, have taken a mechanistic
approach to understanding how abiotic factors other
than resource supply impact community invasibility.
Correlational studies have shown that exotic species
richness and abundance generally decrease with increasing abiotic stress (Forcella and Harvey 1983, D’Antonio
1993, King and Grace 2000, Harrison et al. 2001,
Holway et al. 2002, Williamson and Harrison 2002,
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PLANT INVASIONS OF VERNAL POOLS
Gerhardt and Collinge 2003, Seabloom and van der
Valk 2003). Collectively, these studies suggest that
invasions of exotic species are directly precluded by
unfavorable abiotic conditions. Abiotic constraints may
also indirectly affect invasions by altering the native
communities encountered by invading species.
In contrast, biotic resistance to invasions has been
relatively well studied. Exotic species may be excluded
from less invaded communities by the lack of vacant
niches, competition from more diverse species assemblages, the presence of predators and pathogens, or the
lack of disturbances that reduce competition for
resources (reviewed in Mack et al. [2000]). Much of
the theoretical and empirical research on biotic resistance has focused on the role of species diversity in
determining community invasibility (reviewed in Levine
and D’Antonio [1999]). However, other measures of
community structure and composition, such as interaction strength and species identity, have been studied less
but may predict community invasibility better (Robinson and Dickerson 1984, Robinson and Edgemon 1988,
D’Antonio 1993, Robinson et al. 1995, McGrady-Steed
et al. 1997, Crawley et al. 1999, Lavorel et al. 1999).
Abiotic constraints and biotic resistance may also
interact to determine community invasibility in one of
two ways. First, the strength of biotic interactions may
differ among sites along abiotic gradients. For example,
interactions such as competition are thought to decrease
in importance as abiotic stress increases (Grime 1973,
1979, but see Wiens 1977). Alternatively, abiotic stress
and biotic interactions may determine invasibility at
different sites along environmental gradients (Connell
1961, Gurevitch 1986, Hacker and Bertness 1999,
Greiner La Peyre et al. 2001). However, few studies
have examined the importance of interactions between
abiotic and biotic factors in determining community
invasibility. These few studies have shown that the
outcomes of competitive interactions among native and
exotic species depend on abiotic conditions (David 1999)
and that abiotic factors and interactions with competitors and herbivores prevent invasions at different sites
within a community (D’Antonio 1993).
There is a long history in ecology of using environmental gradients to study the relative importance of
abiotic and biotic factors in determining community
structure and composition (e.g., Connell 1961, Gurevitch 1986). Environmental gradients also provide a
unique opportunity to study the abiotic and biotic
mechanisms determining community invasibility for
several reasons. First, environmental gradients are
widespread in nature and are often correlated with
patterns of invasion (e.g., light gradients at forest edges
[Brothers and Spingarn 1992, Goldblum and Beatty
1999], soil gradients in serpentine grasslands [Harrison
et al. 2001, Williamson and Harrison 2002], salinity
gradients in salt marshes [Dethier and Hacker 2005], and
inundation gradients in freshwater wetlands [Gerhardt
and Collinge 2003, Seabloom and van der Valk 2003]).
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Although the specifics may differ, the general mechanisms determining invasibility are likely to be similar
across these and other environmental gradients (D’Antonio 1993). Second, because the contrasting abiotic and
biotic conditions often occur in close proximity, there
are unlikely to be the enormous differences in propagule
pressure that commonly occur among more distant sites
(Crawley et al. 1996, Mack et al. 2000). Finally, the
intensity and frequency of many natural and human
disturbances do not differ across these gradients. Thus,
environmental gradients provide a unique opportunity
to study community invasibility across a range of abiotic
and biotic conditions without the confounding effects of
propagule pressure and disturbance history.
In this study, we used the environmental gradient
found in vernal pools to examine the relative importance
of the abiotic and biotic mechanisms determining
community invasibility. Vernal pools are seasonal
wetlands occurring in shallow depressions on slowly
permeable or impermeable substrates. In the Central
Valley of California, vernal pools typically flood during
winter (December–March) and are dry during summer
and autumn (April–November). Vernal pools are
characterized by strong gradients in abiotic and biotic
conditions. The abiotic gradient is most evident as
differences in depth and duration of flooding, but other
associated physical and chemical gradients include
timing and predictability of flooding, winter soil
temperatures, soil pH and salinity, and nutrient availability (Linhart 1976, Holland and Jain 1988, Holland
and Dains 1990, Bliss and Zedler 1998, Gerhardt and
Collinge 2003). Paralleling this abiotic gradient is a
biotic gradient from barely invaded plant communities
in the pools to highly invaded communities at the edges
of the pools and in the surrounding grasslands (Holland
and Jain 1981, 1988, Ferren et al. 1998, Pollak and Kan
1998, Bauder 2000, Gerhardt and Collinge 2003).
Because these gradients occur across scales of only a
few meters, there are not significant differences in
propagule pressure (Gerhardt 2003). Furthermore,
natural disturbances, such as wildfire, were not historically important in the Central Valley (Keeley 2002), and
anthropogenic disturbances, such as discing and mowing, often occurred uniformly across both vernal pools
and the surrounding grasslands (e.g., Biosystems Analysis 1994). Vernal pools typically support a unique and
highly endemic flora and fauna (Stone 1990, Baskin
1994). However, 93–97% of the vernal pools in
California have been lost to agricultural and urban
development. Thus, remaining vernal pool habitats are a
high priority for conservation.
In this study, we used a greenhouse experiment
simulating the environmental gradient found in vernal
pools to better understand the abiotic and biotic
mechanisms determining community invasibility and
the implications for conservation and management of
natural communities. Specifically, we invaded plant
communities differing in richness, identity, and abun-
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FRITZ GERHARDT AND SHARON K. COLLINGE
Ecological Applications
Vol. 17, No. 3
TABLE 1. Characteristics of five exotic and three native species used in a greenhouse experiment examining abiotic and biotic
resistance to plant invasions.
Species
Common name
Family
Functional group
Habitat
Exotic species
Brassica rapa
Centaurea solstitialis
Hordeum marinum
Lolium multiflorum
Vicia villosa
wild mustard
yellow starthistle
wild barley
Italian ryegrass
hairy vetch
Brassicaceae
Asteraceae
Poaceae
Poaceae
Fabaceae
early annual forb
late annual forb
annual grass
annual grass
annual legume
grasslands
grasslands
deep pools
pool edges
grasslands
Native species
Deschampsia danthonioides
Lasthenia conjugens
Layia chrysanthemoides
purple hairgrass
Contra Costa goldfields
tidy tips
Poaceae
Asteraceae
Asteraceae
annual grass
early annual forb
early annual forb
shallow pools
deep pools
shallow pools
Notes: Nomenclature and taxonomic and functional groups follow Hickman (1993); habitat information follows Gerhardt and
Collinge (2003) and Gerhardt (2003).
dance of native plants and depth of inundation to
measure the effects of these abiotic and biotic factors on
the growth, reproduction, and survival of five exotic
plant species. This experiment allowed us to address five
questions: (1) What are the direct effects of abiotic
constraints and biotic resistance on community invasibility? (2) What are the indirect effects of abiotic
constraints, as mediated by biotic resistance, on
invasibility? (3) Do abiotic constraints and biotic
resistance interact to determine invasibility? (4) What
components of community structure and composition
best predict biotic resistance to invasions? (5) Which life
history stages (e.g., growth, reproduction, or survival)
are impacted most by abiotic constraints and biotic
resistance? By examining multiple species representing
different taxonomic and functional groups, we were able
to make general inferences about community invasibility, rather than ones specific to a single species.
METHODS
To quantify the effects of inundation and interactions
with neighbors on exotic plant performance, we used a
full factorial design in which water depth and different
combinations of native species were the independent
factors. Five exotic and three native species, representing
multiple taxonomic and functional groups, were used in
this experiment (Table 1). All species, except L.
conjugens, which is a federally listed endangered species,
commonly occur in the Central Valley. We used these
particular species because they represented the range of
distributions observed in the field and because they were
sufficiently abundant to provide seeds for this experiment. Because no native species were widespread or
abundant in the surrounding grasslands, we were limited
to using native species associated with vernal pools,
although two of the three species (D. danthonioides and
L. chrysanthemoides) were more abundant at the edges
of the pools. In addition, few exotic species were more
abundant in vernal pools than the surrounding grasslands (Gerhardt and Collinge 2003), so we included only
one of these species in this experiment (H. marinum). To
avoid sampling effects, we used each of the three native
species in one-species treatments, all three combinations
of two native species in the two-species treatments, and
all three native species in the three-species treatment.
Total density and mass of native plants were not
controlled but were allowed to vary naturally in
response to growing conditions. For each exotic species,
multiple replicates of each neighbor treatment were
placed at each of three water depths (þ6, 0, and 7 cm).
The experiment was conducted in a climate-controlled
greenhouse at the University of Colorado in Boulder,
Colorado, USA. The greenhouse was configured to
approximate winter climate conditions in the Central
Valley. Temperatures were maintained initially at 158–
218C during the day and 28–108C during the night but
gradually increased as the season progressed. Light was
maintained at ambient levels, since the greenhouse is
located at a similar latitude to the northern Central
Valley (40801 0 N and 38815 0 N, respectively). For this
experiment, we used topsoil collected near Boulder,
Colorado. We did not use vernal pool soils for logistical
reasons as well as to avoid disturbing the pools. The
greenhouse soil was generally coarser and had less
organic matter and higher pH, nitrates, and soluble salts
than vernal pool soils (Gerhardt 2003). However, both
soils represented generally benign growing conditions
without severe nutrient limitations, and these differences
were unlikely to alter the results of this experiment. To
simulate different water depths, we placed 15 plastic
pots (9.2 3 9.2 3 8.9 cm) on bricks in plastic, rectangular
tubs (27.5 3 53.5 3 27.5 cm) filled with 15 cm of water.
Five pots each were placed so that the soil surface was 6
cm above, even with, and 7 cm below the water level
(actual depths [means 6 SD] were 6.2 6 0.5 cm and
0.4 6 0.5 cm above and 6.6 6 0.6 cm below the water
surface). Three pots, one at each depth, were assigned to
each exotic species. Each pot contained a different
neighbor richness treatment (one, two, or three species)
and a different combination of native species, so that
each tub contained three of the seven possible neighbor
treatments for each exotic species. Locations of exotic
species and water depths were randomly assigned in
each tub.
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925
FIG. 1. Numbers of significant statistical tests analyzing performance of five exotic plant species in relation to inundation and
neighborhood treatments in a greenhouse experiment examining abiotic and biotic resistance to plant invasions. The height of each
bar indicates the total number of significant tests, which are partitioned into the five measures of performance contributing to that
total.
All seeds used in this experiment were collected in
April–May and August 2002 at Travis Air Force Base
(Travis AFB) in the Central Valley of California (site
described in Gerhardt and Collinge [2003]) and were
stored in paper envelopes under cool, dry conditions
until planting. Because many of these species show
genetic and phenotypic variation both within and
among populations (Linhart and Baker 1973, Linhart
1974, 1976, 1988, Collinge et al. 2003), we collected seeds
from across the vernal pools and surrounding grasslands
at Travis AFB and pooled all seeds of each species
before planting. During January 2003, we planted 3–5
seeds of one exotic species (hereafter, referred to as the
‘‘focal’’ plant or species) and 20–30 seeds of 1–3 native
species (hereafter, referred to as the ‘‘neighboring’’
plants or species) in each pot. After 3–4 weeks, we
thinned the focal plants so that only the individual
growing nearest the center of the pot remained.
Neighboring plants were not thinned or supplemented,
and density and mass were allowed to vary naturally in
response to growing conditions. All pots were placed at
their assigned water depths 5 weeks after planting and
were inundated for 38 d, which represents an intermediate duration of inundation in the vernal pools at
Travis AFB (S. K. Collinge, unpublished data). After
38 d, the tubs were drained, but pots were watered
regularly so that the soil remained moist for the
remainder of the experiment. The experiment was
terminated in June 2003, when all species, except
C. solstitialis, were beginning to senesce. At that time,
we measured numbers of leaves, heights, and numbers of
inflorescences of all surviving focal plants and numbers
of individuals of each neighboring species (see Plate 1).
We then harvested the focal and neighboring plants,
oven-dried them at 588C until they reached a stable
mass, and measured total mass of each focal plant and
all neighboring plants collectively.
To characterize plant neighborhoods, we used fixedeffects ANOVA to analyze the final richness, density,
and mass of neighbors as a function of focal species,
water depth, and initial neighbor richness and identity.
To measure the direct effects of inundation, water depth
was analyzed separately. In contrast, all analyses of
plant neighborhood included water depth as a covariate
to remove the variance explained by that factor. We
analyzed survival by the likelihood ratio v2 test (water
depth and neighbor richness and identity) or logistic
regression (neighbor density and mass). The three
measures of growth and reproduction (total mass,
number of inflorescences, and leaf : height ratio) were
analyzed by MANOVA (water depth and neighbor
richness and identity) or MANCOVA (neighbor density
and mass). All analyses were conducted with SYSTAT
6.0.1 (SPSS 1996). Analyses in which P , 0.05 were
considered significant. Unless otherwise noted, values
presented in the text are means 6 SE.
RESULTS
Water depth impacted more measures of exotic plant
performance than plant neighborhood or interactions
between water depth and plant neighborhood (Fig. 1,
Appendix A). Water depth affected 17 of 24 measures of
performance, including survival, growth, and reproduction. Survival of B. rapa, C. solstitialis, and V. villosa all
decreased with increasing depth, and no individuals of
B. rapa or C. solstitialis survived at the greatest depth
(Fig. 2A). In contrast, survival of H. marinum and
L. multiflorum was unaffected by water depth. The
overall MANOVAs, which included all measures of
growth and reproduction, were significant for all five
species (Appendix A). Total mass of C. solstitialis,
H. marinum, and L. multiflorum all decreased with
increasing depth (Fig. 2B). Numbers of inflorescences of
H. marinum and L. multiflorum also decreased with
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FRITZ GERHARDT AND SHARON K. COLLINGE
Ecological Applications
Vol. 17, No. 3
FIG. 2. Performance of five exotic plant species in relation to water depth in a greenhouse experiment examining abiotic and
biotic resistance to plant invasions. Water depth increases from left to right. In panels (B)–(D), values are means 6 SE. In panel
(C), numbers of inflorescences are presented on a logarithmic scale. No individuals of B. rapa or C. solstitialis survived in the 7 cm
treatment, and no inflorescences were produced by C. solstitialis in any treatment.
increasing depth (Fig. 2C). Finally, leaf : height ratios of
three species (B. rapa, H. marinum, and V. villosa)
decreased with increasing depth (Fig. 2D).
Plant neighborhood primarily affected growth and
reproduction (Fig. 1, Appendix A). However, the four
measures of plant neighborhood differed greatly in their
effects, as neighbor density and mass impacted more
measures of performance than neighbor richness or
identity. Neighbor density, which affected seven of 24
measures of performance, affected growth and repro-
duction but not survival. In most instances, growth and
reproduction decreased as neighbor density increased:
total mass of H. marinum (Fig. 3A) and total mass and
numbers of inflorescences of L. multiflorum (Fig. 3B, C).
In contrast, total mass and numbers of inflorescences of
B. rapa increased as neighbor density increased (Fig.
3D, E). Neighbor mass, which affected nine of 24
measures of performance, was the only measure of plant
neighborhood to impact survival as well as growth and
reproduction. For both B. rapa and C. solstitialis,
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PLANT INVASIONS OF VERNAL POOLS
neighbor mass was greater for surviving individuals than
for those that died (Fig. 4A, B). In all instances, growth
and reproduction decreased as neighbor mass increased:
total mass of C. solstitialis (Fig. 4C) and total mass and
numbers of inflorescences of H. marinum (Fig. 4D, E)
and L. multiflorum (Fig. 4F, G). Neighbor richness
affected only one of 24 measures of performance: total
mass of L. multiflorum decreased with increasing
neighbor richness (one species, 3.3 6 0.3 g; two species,
3.0 6 0.3 g; three species, 2.2 6 0.3 g). Finally, neighbor
identity affected only four of 48 measures of performance (Appendix A). In the one-species treatments,
total mass of C. solstitialis was ranked Deschampsia .
Layia . Lasthenia (Appendix B). In the two-species
treatments, total mass of L. multiflorum was ranked
Lasthenia–Layia . Deschampsia–Lasthenia . Deschampsia–Layia.
Only one of the 95 interaction terms between water
depth and the four measures of plant neighborhood
were significant (data not presented). For B. rapa, the
interaction between water depth and neighbor richness
was significant for leaf : height ratio (F ¼ 4.943, df ¼ 1,
32, P ¼ 0.033): at the shallowest depth, leaf : height ratios
decreased with increasing richness, but, at the intermediate depth, leaf : height ratios increased with increasing
richness.
Indicating the efficacy of our methods, the plant
neighborhoods experienced by focal plants differed
among focal species, water depth, and neighbor
treatments (Appendix C). Neighbor mass was greatest
for C. solstitialis and V. villosa and least for H. marinum
and L. multiflorum (Appendix D). Neighbor identity
also differed among focal species, as one- and twospecies treatments containing Deschampsia were underrepresented for all species, except V. villosa. Final
richness and mass were greater at lesser water depths
(Appendix D). Final richness, density, and mass
increased with increasing initial neighbor richness
(Appendix D). Neighbor identity also differed among
initial richness treatments, primarily because one-species
treatments included fewer Deschampsia samples. Final
richness, density, and mass also differed among neighbor identity treatments. All three measures were least in
the Layia-only treatment and greatest in the two- and
three-species treatments containing both Deschampsia
and Lasthenia (Appendix E). Furthermore, density was
greatest in all four treatments containing Lasthenia, and
mass was greatest in all four treatments containing
Deschampsia.
DISCUSSION
In this experiment, we simulated an environmental
gradient to better understand the abiotic and biotic
mechanisms determining community invasibility. Based
on our results, we conclude that both abiotic constraints
and interactions with the native community play
important but distinct roles in determining invasibility
along this gradient. However, because inundation
927
FIG. 3. Performance of three exotic plant species in relation
to density of native neighbors in a greenhouse experiment
examining abiotic and biotic resistance to plant invasions. Only
significant relationships are shown (P , 0.05; see Appendix A).
Measures of performance include total mass and number of
inflorescences shown in relation to the number of native
neighbors. Lines are regression lines.
greatly reduced all measures of performance, including
survival, but interactions with neighboring plants
primarily affected growth and reproduction, abiotic
constraints played the dominant role in determining
invasibility. In addition, biotic resistance to invasions
was best predicted by neighbor density and mass, rather
than by neighbor richness or identity. Surprisingly,
interactions between abiotic and biotic factors had few
significant effects on exotic plant performance and
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FRITZ GERHARDT AND SHARON K. COLLINGE
Ecological Applications
Vol. 17, No. 3
FIG. 4. Performance of four exotic plant species in relation to mass of native neighbors in a greenhouse experiment examining
abiotic and biotic resistance to plant invasions. Only significant relationships are shown (P , 0.05; see Appendix A). Measures of
performance include survival, total mass, and number of inflorescences shown in relation to the final mass of native neighbors. In
panels (A) and (B), values are mean mass 6 SE of native neighbors for exotic plants that survived or died during the experiment. In
panels (C)–(G), lines are regression lines.
played little, if any, role in determining invasibility in
this system. In the sections that follow, we discuss these
results in terms of the responses of individual species,
mechanisms underlying abiotic and biotic resistance to
invasions, implications for hypotheses and models of
community invasibility, and consequences for the
conservation and management of natural communities.
Responses of individual species
Based on their responses to the experimental treatments, the five species segregated into two distinct
groups that broadly paralleled their distributions in
vernal pools and the surrounding grasslands. Three
species (B. rapa, C. solstitialis, and V. villosa) suffered
high mortality due to inundation (Fig. 2A) but were
generally not affected by neighboring plants (Appendix
A). In the field, these three species only occur at the
edges of pools and in the surrounding grasslands
(Gerhardt 2003, Gerhardt and Collinge 2003). These
three species likely represent the majority of exotic
species, which are unable to invade sites characterized by
stressful abiotic conditions.
In contrast, the two species whose survival was least
affected by inundation (H. marinum and L. multiflorum)
were also the most impacted by interactions with
neighboring plants. Both species had high rates of
survival (.94%) at all water depths, but their growth
and reproduction generally decreased with both increasing inundation (Fig. 2B, C) and increasing abundances
of neighbors (Figs. 3–4). However, the distributions of
these two species differ greatly in the field (Gerhardt and
Collinge 2003). Lolium multiflorum occurs throughout
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PLANT INVASIONS OF VERNAL POOLS
929
PLATE 1. Sara Jo Dickens, currently a graduate student at the University of California–Riverside, measures plant growth for
exotic plants being grown in a greenhouse experiment examining abiotic and biotic resistance to plant invasions. Photo credit: F.
Gerhardt.
the vernal pools and surrounding grasslands but is most
abundant at pool edges. In contrast, H. marinum is most
abundant at greater water depths in the pools. This
difference in distribution may reflect different strategies
for avoiding competition. Hordeum marinum may avoid
competition by growing at greater water depths, where
neighbors are less abundant (Appendix D), whereas
L. multiflorum may be making a trade-off between
avoiding inundation at greater water depths while
avoiding more intense competition outside the pools,
where neighbors are more abundant.
These patterns suggest that the species most impacted
by abiotic constraints (i.e., those that suffered the
greatest mortality due to inundation) may be less
sensitive to biotic interactions. In contrast, species that
are less sensitive to abiotic constraints may be more
sensitive to biotic interactions, especially the negative
effects of competition. This pattern corresponds well to
the plant ecological strategies proposed by Grime
(1979). Species that are stress-tolerant are likely to be
poor competitors, and those that are good competitors
are likely to be less tolerant of stress.
Direct effects of abiotic constraints
This experiment provides strong experimental evidence that abiotic constraints directly limit community
invasibility. Thus, our results strongly support the
abiotic constraints hypothesis, which proposes that
exotic species are unable to tolerate abiotic conditions
in less invaded communities (Fox and Fox 1986,
Rejmánek 1989, Lodge 1993, Ewel et al. 1999).
Furthermore, our results also support several models
that propose that exotic species are less likely to invade
communities characterized by stressful abiotic conditions, whether imposed by physical site characteristics,
microclimate, or soil and nutrient properties (Moyle and
Light 1996, Lonsdale 1999, Alpert et al. 2000, Davis
et al. 2000). Such constraints are likely to be most
pronounced along environmental gradients encompassing extreme abiotic conditions, especially those not
encountered by the majority of invading species in their
native ranges (Moyle and Marchetti 2006).
Abiotic constraints, such as inundation, may limit
invasibility by reducing survival rather than growth or
reproduction (although reduced reproduction may also
be important when dispersal is limiting). In this study,
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FRITZ GERHARDT AND SHARON K. COLLINGE
B. rapa, C. solstitialis, and V. villosa all suffered high
mortality at greater water depths (Fig. 2A). Other
studies have shown that inundation reduces the survival
of other exotic plants invading vernal pools (e.g.,
Hypochaeris glabra L. and Erodium botrys (Cav.) Bertol.
[Bauder 1987]) and other wetlands (e.g., Imperata
cylindrica (L.) Beauv. [King and Grace 2000]). Furthermore, Holway et al. (2002) found that high temperatures
reduced the survival and, consequently, the ability of
Argentine ants (Linepithema humile Mayr) to invade new
habitats. Thus, abiotic constraints may limit invasibility
by allowing survival of only those species with the
appropriate morphological and physiological traits.
Many species native to stressful habitats have evolved
mechanisms to cope with abiotic stressors, such as
inundation (Linhart and Baker 1973, Keeley 1990). In
contrast, most exotic species currently present in the
regional species pool do not have such mechanisms. In
this study, the one possible exception was H. marinum,
which was one of the two species least affected by
inundation (Fig. 2). When inundated, H. marinum
develops high root porosity and barriers to radial
oxygen loss, two traits that enhance growth and survival
under anaerobic conditions (McDonald et al. 2001).
Such mechanisms may allow this and other exotic
species (e.g., Lythrum hyssopifolium, which was also
more abundant at greater water depths in vernal pools
[Gerhardt and Collinge 2003]) to invade these stressful
environments. In contrast, the other exotic species
examined in this study, and most other exotic species
in general, likely do not have the morphological and
physiological traits necessary to tolerate inundation or
other extreme abiotic conditions.
Biotic resistance to invasions
In contrast to abiotic constraints, biotic resistance
played a less important role in determining community
invasibility. In this study, plant neighborhoods affected
few measures of performance, and these effects were
generally restricted to growth and reproduction. These
effects may reflect either above- or belowground
competition. Indicating aboveground competition for
light, individual plants allocated more resources to shoot
and height growth when neighbors were present or more
abundant in other experiments (Gerhardt 2003). In
addition, belowground competition for nutrients may be
important because nutrients, although generally occurring at high levels in vernal pools (Gerhardt and
Collinge 2003), may be made less available by inundation (Crawford 1992).
Although biotic interactions had relatively few effects
on exotic plant performance, the individual measures of
community structure and composition did differ in their
impacts. In particular, neighbor abundance, whether
measured as density or mass, affected more measures of
performance than neighbor richness or identity (Fig. 1).
This result suggests that neighbor abundance is a better
predictor of biotic resistance to invasions than neighbor
Ecological Applications
Vol. 17, No. 3
richness or identity, possibly because abundance more
accurately describes the intensity of competition for and
availability of unused resources. Furthermore, in these
annual grasslands, standing biomass reflects overall
productivity, and productivity has been suggested to
play an important role in determining biotic resistance
to invasions in other systems (Smith and Knapp 1999).
Other studies have also shown that the density of
neighbors affected recruitment of invading species
(Crawley et al. 1999, Lavorel et al. 1999) and that
dominant species that interact strongly with other
species are likely to preclude invasions (Robinson and
Dickerson 1984, Robinson and Edgemon 1988, Robinson et al. 1995, McGrady-Steed et al. 1997, Smith and
Knapp 1999).
Thus, this study questions the importance of species
diversity in determining biotic resistance to invasions,
despite the plethora of studies that have found strong
relationships between diversity and invasibility (reviewed in Levine and D’Antonio [1999]). There are
several possible explanations for this contradiction.
First, as noted above, biotic resistance to invasions
likely reflects the competitive environment faced by
invaders, and neighbor abundance may better predict
intensity of competition than does neighbor diversity.
Second, the narrow range of neighbor richness examined
in this study (1–3 species) may have limited our ability to
detect the effects of diversity. However, other studies
(e.g., Tilman and Downing 1994, Tilman et al. 1997)
have shown that the functional effects of species
diversity are typically most pronounced at lower ranges
of species richness (e.g., ,10 species). Furthermore,
Lavorel et al. (1999) examined a broader range of species
richness (3–18 species) and also concluded that abundance was more important than diversity in determining
invasibility. Third, the effects of diversity in other
studies may actually reflect other aspects of community
structure and composition that are correlated with
diversity. For example, in this study, both neighbor
density and mass were positively correlated with
neighbor richness (Appendix D). Although many studies
examining the relationship between diversity and invasibility have not reported these correlations, the few that
have have generally found positive correlations between
neighbor richness and abundance (e.g., Stachowicz et al.
1999, Levine 2000). Thus, it may be these differences in
abundance, rather than diversity, that actually determine community invasibility.
Finally, the effects of diversity on invasibility may
depend on the functional diversity of the community
being invaded, especially relative to that of invading
species. Specifically, species that are functionally similar
are more likely to compete for the same resources and to
occupy similar niches than dissimilar species. In this
study, the exotic grass L. multiflorum grew larger when
grown with native composites (L. conjugens and
L. chrysanthemoides) than when grown with the native
grass D. danthonioides (Appendix B). In contrast, the
April 2007
PLANT INVASIONS OF VERNAL POOLS
exotic composite C. solstitialis grew larger when grown
with the native grass than when grown with either of the
native composites, even though C. solstitialis is a lateseason annual and L. conjugens and L. chrysanthemoides are early-season annuals (Appendix 2). Other
studies have shown that recruitment of exotic species is
greatly diminished when invaders occupy similar functional or taxonomic groups as native species in the
community being invaded (e.g., Lavorel et al. 1999,
Fargione et al. 2003).
Conclusions and implications
In summary, the results presented here suggest that
community invasibility, at least along the environmental
gradient examined in this study, is determined primarily
by abiotic constraints and secondarily by interactions with
the native biota. Few studies have examined the relative
importance of abiotic constraints and biotic resistance in
determining invasibility. Those few studies have also
found that abiotic conditions play the dominant role in
determining community invasibility (e.g., riparian tussock
plant communities [Levine 2000]; coastal chaparral and
sage scrub ant communities [Holway et al. 2002]; estuarine
marsh grass communities [Dethier and Hacker 2005]).
This dominant role of abiotic constraints will likely hold
true across vernal pool and similar environmental
gradients encompassing abiotic conditions not typically
encountered by invading species in their native ranges
(Moyle and Marchetti 2006). In contrast, biotic interactions are likely to have little or no impact on invasibility
across broad gradients of environmental conditions,
although they may be locally important in more benign
environments where abiotic constraints are not limiting.
Thus, across broader regions and landscapes, abiotic
constraints likely act as coarse filters limiting the
invasibility of more stressful environments, and biotic
resistance acts as a fine filter reducing invasibility only in
more favorable environments.
This study has important implications for the
conservation and management of natural communities.
Based on this and other studies (e.g., Harrison et al.
2001, Williamson and Harrison 2002, Dethier and
Hacker 2005), it is clear that stressful environments,
whether in vernal pools or along other stress gradients,
are less likely to be invaded than more benign ones, at
least by the majority of invading species. However,
species such as H. marinum that are able to tolerate
stressful abiotic conditions potentially pose grave threats
to conservation of biodiversity, because they are more
likely to invade stressful environments supporting high
rates of endemism and concentrations of rare species
(e.g., vernal pools, serpentine grasslands). These stressful environments also typically support less productive
communities that do not have the abundant cover of
native species that might better resist invasion. Fortunately, as illustrated in this study by H. marinum, these
stress-tolerant species are also more likely to be
negatively impacted by competition from native species.
931
Thus, by manipulating environmental stressors and
maintaining healthy communities of stress-tolerant
native species, managers and conservationists may be
able to exclude invasions of most exotic species from
these environments.
In contrast, this study suggests that, in more benign
environments, healthy and productive native communities are likely to be more resistant to invasion than less
productive communities. Unfortunately, in these environments, species such as B. rapa, C. solstitialis, and
V. villosa that are stress-intolerant but good competitors
may be more likely to overcome resistance from native
species, even in more productive communities. These
results also suggest that loss of native biomass may be
one of the mechanisms whereby disturbances increase
the invasibility of native communities. Thus, managers
and conservationists may be able to control, or at least
reduce, invasions in more benign environments by
maintaining healthy and productive communities with
their full complement of native species, by minimizing or
eliminating disturbances that reduce native biomass, and
by encouraging the rapid recovery of native communities following disturbance.
ACKNOWLEDGMENTS
We thank Susan Beatty, Carl Bock, Marcel Holyoak, Sharon
Lawler, Yan Linhart, Jaymee Marty, Kevin Rice, and Tim
Seastedt for valuable suggestions and criticisms throughout this
study. Tom Lemieux and Charles Grayless provided greenhouse space and many valuable suggestions for conducting this
experiment. Sara Jo Dickens, Kasey Barton, Caroline Mitchell,
Jenny Ramp, and Eric Toonder provided valuable assistance in
the greenhouse. Susan Beatty, Carl Bock, Sharon Lawler, Yan
Linhart, Tim Seastedt, and two anonymous reviewers provided
valuable comments on earlier versions of this manuscript. This
research was supported by the Air Force Center for Environmental Excellence (grant F41624-01-M-8903 to S. K. Collinge),
the U.S. Fish and Wildlife Service (contract 101811M575 to
S. K. Collinge), and the Department of Ecology and
Evolutionary Biology and the Graduate School at the
University of Colorado.
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APPENDIX A
A table showing statistical relationships between performance and water depth and neighbor richness, density, mass, and identity
(Ecological Archives A017-034-A1).
APPENDIX B
A table showing significant relationships between growth of Centaurea solstitialis and Lolium multiflorum and neighbor identity
(Ecological Archives A017-034-A2).
APPENDIX C
A table showing statistical relationships between experimental treatments and characteristics of plant neighborhoods (Ecological
Archives A017-034-A3).
APPENDIX D
A figure showing significant relationships between plant neighborhood and focal species, water depth, and initial neighbor
richness (Ecological Archives A017-034-A4).
APPENDIX E
A table showing final richness, density, and mass of neighbors in relation to neighbor identity (Ecological Archives A017-034A5).