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Oikos 116: 1164 1170, 2007
doi: 10.1111/j.2007.0030-1299.15406.x,
Copyright # Oikos 2007, ISSN 0030-1299
Subject Editor: Lonnie Aarsen, Accepted 8 February 2007
Species evenness and invasion resistance of experimental
grassland communities
W. Brett Mattingly, Rachel Hewlate and Heather L. Reynolds
W. B. Mattingly, R. Hewlate and H. L. Reynolds ([email protected]), Dept of Biology, Indiana Univ., Jordan Hall Room 142,
1001 E. Third Street, Bloomington, IN 47405-7005, USA.
Concern for biodiversity loss coupled with the accelerated rate of biological invasions has provoked much
interest in assessing how native plant species diversity affects invasibility. Although experimental studies
extensively document the effects of species richness on invader performance, the role of species evenness in such
studies is rarely examined. Species evenness warrants more attention because the relative abundances of species
can account for substantially more of the variance in plant community diversity and tend to change more rapidly
and more frequently in response to disturbances than the absolute numbers of species. In this study, we
experimentally manipulated species evenness within native prairie grassland mesocosms. We assessed how
evenness affected primary productivity, light availability and the resistance of native communities to invasion.
The primary productivity of native communities increased significantly with species evenness, and this increase
in productivity was accompanied by significant decreases in light availability. However, evenness had no effect
on native community resistance to invasion by three common exotic invasive species. In this study, niche
complementarity provides a potential mechanism for the effects of evenness on productivity and light
availability, but these effects apparently were not strong enough to alter the invasibility of the experimental
communities. Our results suggest that species evenness enhances community productivity but provides no
benefit to invasion resistance in otherwise functionally diverse communities.
The study of biological invasions has a long history in
ecology as a key avenue of insight into the processes
controlling species distributions and abundances and
the structure and functioning of ecosystems (Elton
1958). Furthermore, biological invasions are occurring
at an unprecedented rate and posing serious threats to
natural and managed systems worldwide, often resulting in substantial ecological and economic losses
(Vitousek et al. 1997). For example, invasive species
can disrupt ecosystem processes by displacing native
species, altering patterns of resource use and modifying
disturbance regimes (Mack and D’Antonio 1998, Mack
et al. 2000), and these ecological consequences of
invasions jeopardize native biodiversity and associated
ecosystem services (Chapin et al. 2000). Invasive species
also cause substantial economic losses by reducing the
output of plant and animal production of managed
systems and warranting costs associated with management practices (Pimentel et al. 2000).
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Focusing on attributes of invaded communities, a
critical question addresses why communities vary in
their resistance to invasions (Lonsdale 1999). Elton
(1958) hypothesized that a community’s resistance to
invasion increases with species diversity. Modern
ecologists have provided a mechanistic basis for Elton’s
idea, proposing that species-rich communities either
offer fewer vacant niches (niche complementarity effect
of native species richness) or a greater probability that
an invader will be competitively excluded by a superior
competitor (sampling effect of native species richness)
(Tilman 1999, Wardle 2001, Fargione and Tilman
2005). Tilman (1999) demonstrated that both of these
diversity effects operate through resource reduction,
with higher native species richness leading to greater
resource reduction, greater community productivity,
and lower invasibility in both heterogeneous (for niche
complementarity) and homogenous (for the sampling
effect) environments.
A substantial body of work testing the relationship
between species richness and invasibility has emerged,
with variable results that are in part due to the differing
scales and contexts of studies (reviewed by Levine and
D’Antonio 1999). However, species richness is not the
only measure of community diversity and does not
always correlate positively with other measures (e.g.
species evenness), which may be a contributing factor to
the variable results of richness invasibility studies
(Wilsey et al. 2005). Species evenness, or the relative
abundances of species in a community, has rarely been
considered in studies of community invasibility but
warrants more attention for a number of reasons.
Experimental studies manipulating species richness
typically impose high levels of initial species evenness
(Schwartz et al. 2000), but natural plant communities
often exhibit low evenness (Weiher and Keddy 1999).
Furthermore, relative abundances of species can account
for substantially more of the variance in plant community diversity than does species richness (Stirling and
Wilsey 2001, Wilsey et al. 2005) and tend to change
more rapidly and more frequently in response to human
activities and other disturbances than the absolute
numbers of species within a community (Chapin
et al. 2000). In addition, theoretical work predicts
that evenness affects the extent to which niche
complementarity results in exploitation of resourcebased niches, with greater evenness resulting in greater
resource drawdown and thus greater productivity and
less opportunity for successful invasion (Nijs and Roy
2000), though empirical studies testing this prediction
offer little support to date (Polley et al. 2003).
To our knowledge, only one study has used a
manipulative experiment to explicitly test the relationship between species evenness and the susceptibility of a
community to invasion. Wilsey and Polley (2002)
demonstrated that increased evenness of grassland plots
resulted in a decrease in the natural recruitment of
native species, though the response depended largely on
the identity (e.g. monocotyledonous vs dicotyledonous
invaders) of the recruiting species. Here we report the
results of a greenhouse experiment designed to test
whether native grassland species evenness promotes
greater native community productivity, reduced light
availability, and greater resistance to exotic invaders.
Methods
Study species
We assembled native communities from a pool of 25
species common to mesic prairies of the mid-western
United States. Species within this pool were divided
among five functional groups: C3 grasses (Agropyron
smithii, Bromus kalmii , Elymus canadensis , Elymus
virginicus and Glyceria grandis ); C4 grasses (Andropogon
gerardii, Panicum virgatum , Schizachyrium scoparium ,
Sorghastrum nutans and Spartina pectinata); composites
(Aster novae-angliae , Coreopsis tripteris , Echinacea purpurea , Heliopsis helianthoides and Rudbeckia hirta );
legumes (Amorpha canescens , Astragalus canadensis ,
Chamaecrista fasciculata , Desmanthus illinoensis and
Desmodium canadense ); and a miscellaneous category
denoted as other (Asclepias tuberosa, Monarda fistulosa ,
Penstemon digitalis , Prunella vulgaris and Pycnanthemum tenuifolium ). Our study also included three exotic
plant species: Lolium arundinaceum , Melilotus alba and
Rumex crispus , all of which are common invaders of
mid-western grasslands. Lolium arundinaceum is a
highly persistent, cool-season grass that can substantially reduce grassland biodiversity, especially when
infected by the endophytic fungus Neotyphodium
coenophialum (Clay and Holah 1999). The abundances
of Melilotus alba (a nitrogen-fixing legume) and Rumex
crispus (a non-leguminous forb) are also negatively
correlated with the performance of native species within
grassland communities (Parker et al. 1993, Tracy and
Sanderson 2004). Seeds of native species were obtained
commercially (J. F. New Native Plant Nursery, Walkerton, IN, USA), and seeds of exotics were collected
from naturally growing populations in the mid-west.
Experimental design
Native functional group richness, species richness, and
total planting density were all held constant at five
functional groups, five species, and thirty individuals
per pot, respectively. We established three levels of
native species evenness, with species abundances in the
ratios of 1:1:1:1:6 (low evenness), 1:1:3:5:5 (medium
evenness), and 1:1:1:1:1 (high evenness). Within each
community, individuals were equally spaced, and
species positions were randomized. Each level of
evenness was replicated 30 times, yielding a total of
90 communities. For each replicate, a species representing each functional group was randomly selected from
the corresponding species pool, and then these five
species were randomly assigned to the five species
abundances for each evenness treatment (Fig. 1).
Thus, while all replicate communities contained five
species and five functional groups, the species composition of each replicate, including which species or
functional group was dominant within a given low or
medium evenness replicate, was an independent random draw. Our design automatically excluded the
sampling effect associated with manipulations of species
or functional group richness. Furthermore, by randomizing each of the 90 replicate communities with
respect to species composition and functional group
dominance, our design avoided compositional effects.
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Functional groups:
FG
1
FG
2
FG
3
FG
4
FG
5
spp.
1-5
spp.
6-10
spp.
11-15
spp.
16-20
spp.
21-25
1
Species pools:
2
Position within
evenness ratios:
:
:
:
:
Fig. 1. Experimental communities were randomly assembled for each replicate, whereby a species representing each functional
group was randomly selected from the corresponding species pool (arrow 1), and then these species were randomly assigned to
each of the five species abundances for each evenness treatment (arrow 2). Position within the evenness ratios reflects the
following relative abundances of species for each evenness treatment: 1:1:1:1:6 (low evenness), 1:1:3:5:5 (medium evenness), and
1:1:1:1:1 (high evenness).
Our design therefore favored the detection of evenness
effects per se, such as those that may operate through
enhanced niche complementarity (Nijs and Roy 2000).
To establish an invasion treatment, we transplanted two
individuals of each of the three exotic invasive species
into half of the native communities within each level of
evenness. The pots lacking exotic species served as
controls.
Seedlings of each study species were grown from
cold stratified seed (48C for 10 d in wet sand) sown into
flats of pasteurized soil. Germinating seeds were
maintained at 21 248C with a photoperiod of 14 h
using artificial lighting. Seedlings of both native and
exotic species were transplanted into pots at approximately 4 weeks of age. Thus, our experiment simulated
a restoration context in which native and exotic species
enter plots simultaneously (e.g. from the intentional
seeding of native species into bare soil with recruitment
of exotic species from seed banks or seed dispersal).
The experimental communities were grown in 7.65-l
pots (20 cm diameter 32 cm depth) in an Indiana
Univ. greenhouse facility during the autumn of 2002.
We filled all pots with a 2:1 mixture of medium-fine
sand and old field topsoil that was sieved through 1-cm
mesh. This sand-soil mixture exposed plants to natural
microbial associates and facilitated the harvest of root
biomass. We replaced all seedlings that died within the
first week of transplanting. Experimental pots were
watered and weeded as needed. We positioned all pots
within a complete randomized block design of fifteen
blocks, each containing all six combinations of species
evenness and invasion treatments.
After a 4-month growing season, we counted the
number of surviving individuals of the invasive species
in each pot and harvested the communities. Shoots were
clipped at stem bases, sorted by species, dried to a
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constant weight at 658C, and weighed (91 mg). Due
to the difficulty in separating root tissue by species in
mixtures, we only obtained measurements of total root
biomass per pot. Roots were sieved from pots, washed
in tap water, and processed in the manner described for
the shoots. Prior to harvest of the uninvaded control
pots, we used a ceptometer to measure the level of light
penetration (photosynthetically active radiation, PAR,
measured as mmol m 2s1) into the canopy two cm
above the soil surface in replicate pots from each
evenness level.
Data analysis
Data were analyzed using SYSTAT statistical software
(ver. 10.2, SPSS Inc.). We used general linear models to
test for treatment effects on shoot and total native
biomass (univariate models) and shoot biomass and
survivorship of exotic species (multivariate models), and
to quantify the relationship between shoot biomass
and light penetration in the uninvaded control pots
(regression model). Because each community consisted
of an independent random draw with respect to both
species composition and functional dominance, we
could test for an effect of species evenness but not of
species composition or functional group dominance on
our response variables (Loreau and Hector 2001,
Mikola et al. 2002). We tested assumptions of homogeneity of variance and normality by inspecting
residual plots (normal probability plots, histograms,
and residual-estimate scatter plots). Data were logtransformed to meet the assumptions of ANOVA
(normalized, homoscedastic residuals) and to remove
any artifacts of scale from interaction terms. We used
Results
Native community productivity, measured as total
aboveground plus belowground biomass produced
over the growing season, increased significantly with
evenness in the absence of exotic species (F2,28 4.19,
p0.026; Fig. 2) and was inversely related to light
availability (y 0.04x0.92, R2 0.33, p B0.001).
However, native species evenness had little effect on
community invasibility in our experimental grassland
communities. There was a tendency for invasion to
reduce the final diversity of low but not higher evenness
communities (Fig. 3), but this effect was not significant
(evenness invasion interaction: F2,70 2.15, p 0.124). Furthermore, native aboveground biomass
decreased significantly in the presence of exotic species
(F1,70 11.78, p 0.001) regardless of the level of
evenness (evenness invasion interaction: F2,70 0.46,
p0.633; Fig. 4). Evenness had no effect on the
aboveground biomass or survivorship of any exotic
species (aboveground biomass: Wilks’ lamda F6,52 0.09, p0.997; survivorship: Wilks’ lamda F6,52 1.511, P 0.193; Fig. 5). Melilotus alba was the
dominant invader at all levels of evenness (Fig. 5).
Discussion
Our results suggest that species evenness promotes
grassland productivity and reduces light availability
but is a relatively unimportant determinant of community vulnerability to invasion by three common exotic
Final diversity (Shannon-Weiner H)
the Tukey-Kramer HSD test (Bonferroni-protected) to
make pairwise mean comparisons on significant effects.
a,b
16
12
a
8
4
0
low
medium
high
Species evenness
Fig. 2. Response of native communities (aboveground plus
belowground biomass) to evenness treatments. Data represent
means 1 SE, and different letters indicate significant
differences (p B0.05) among evenness treatments.
1.50
1.00
0.50
0.00
medium
high
Species evenness
Fig. 3. Response of native species diversity (Shannon Weiner H) to evenness treatments in both the presence and
absence of exotic invaders. Data represent means1 SE.
species. The effects of diversity on community properties (e.g. productivity and invasibility) are often
explained by sampling or niche complementarity effects
(Naeem et al. 1994, Tilman et al. 1997, Tilman 1999,
Wardle 2001), but distinguishing between these effects
can be difficult in studies that manipulate species
richness as a surrogate for diversity because the effects
of species richness are easily confounded with those of
species identity (Wilsey and Potvin 2000, Wilsey and
Polley 2002). The design of our study maintained a
constant level of both species and functional group
richness across the evenness treatments and thus
avoided the sampling effects associated with richness
manipulations. Our design also excluded compositional
effects because both species composition and the
identity of the dominant species in each replicate were
randomly selected. Thus, the positive relationship that
Aboveground native biomass (g)
Total native biomass (g)
b
uninvaded
invaded
low
24
20
2.00
16
12
uninvaded
invaded
8
4
0
low
medium
high
Species evenness
Fig. 4. Response of native communities (aboveground biomass) to invasion treatments at each level of evenness. Data
represent means1 SE.
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35
A
Aboveground biomass (g)
30
25
20
15
10
5
Survivorship (No. of individuals)
0
B
Melilotus alba
Rumex crispus
Lolium arundinaceum
2
1
0
low
medium
high
Species evenness
Fig. 5. Response of aboveground biomass (A) and survivorship (B) of exotic invaders to evenness treatments. Data
represents 1 SE.
we observed between evenness and native community
productivity may be best attributed to an effect of niche
complementarity. Theoretical studies predict that complementarity in resource use increases with species
evenness in functionally diverse communities (Nijs
and Roy 2000). Our measurements of light depletion
support this interpretation, suggesting that canopy
space was more completely filled in more even, and
thus more productive, communities. Of the few other
empirical studies to date, Wilsey and Potvin (2000) also
detected a positive relationship between evenness and
aboveground productivity, but negative (Mulder et al.
2004) and neutral (Polley et al. 2003) relationships
have been observed as well.
Although the patterns of productivity and light
depletion in our study suggest that resource use by
native species was more complete under conditions of
high species evenness, this effect of evenness was
apparently not strong enough to resist invasion. Our
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results contrast with studies that manipulate species
richness. Such studies generally show that resistance to
invasion increases with species richness and often
implicate niche complementarity in above- and/or
belowground resource use as a mechanism of invasion
resistance (Naeem et al. 2000, Hector et al. 2001,
Lindig-Cisneros and Zedler 2002). Our study manipulated species evenness while holding richness constant at
five species from five different functional groups.
Certainly, the presence vs absence of species and/or
functional groups achieved via manipulations of richness might be expected to have stronger effects on niche
complementarity and associated drawdown in resource
use than would variation in the abundances of
individuals (achieved via manipulations of evenness).
Of course, our study was a single-season mesocosm
study, and whereas most richness invasibility experiments have also been single-season in length, they have
been conducted at larger scales in the field (Hector et al.
2001). On the other hand, the diversity effects of
resident vegetation are expected to play out at the
localized scale of plant neighborhoods, an expectation
that is supported by both field (Kennedy et al. 2002)
and complementary field and mesocosm studies
(Naeem et al. 2000). To date, however, richness versus
evenness effects on invasibility have not been directly
compared, and too few evenness studies exist to draw
firm conclusions about the importance of evenness or
how its effect might vary with a community’s level of
functional diversity.
Our study was not designed to separate the effects of
the three invaders, and it is possible that the nature of
the evenness invasibility relationship is contingent on
the identity of the invading species. For example,
Wilsey and Polley (2002) found that high species
evenness decreased invasion of grassland by naturallyrecruiting dicotyledonous species, whereas species evenness had a negligible effect on resistance to monocotyledonous invaders. Observational studies of
evenness invasibility relationships have also been variable, demonstrating both positive (Robinson et al.
1995) and negative (Tracy and Sanderson 2004, Tracy
et al. 2004) results, and suggesting that invasibility can
also be contingent upon the identity of the dominant
native species within low-evenness communities
(Crawley et al. 1999, Smith and Knapp 1999, van
Ruijven et al. 2003, Smith et al. 2004). In our study,
invader biomass was dominated by the nitrogen-fixer
Melilotus alba . Nitrogen fixation can provide a strong
competitive advantage to exotics in nutrient-poor soils,
especially when the ability to fix nitrogen is absent in
the native community (Vitousek et al. 1987, Vitousek
and Walker 1989, Musil 1993). Although all of our
native communities contained native nitrogen fixers, it
is possible that nitrogen-fixing ability varied among
species. Escape from herbivores or pathogens (Tilman
1999), for example, might allow exotic invasives to
allocate relatively more resources than native species to
nitrogen-fixing symbionts. Quantification of nitrogenfixing associations and nitrogen content in plants and
soil would be helpful in addressing these hypotheses.
More generally, studies are needed to evaluate how the
identities of both the invaders and the dominant
residents affect the relationship between species evenness, above- and belowground resources, and community invasibility.
In conclusion, results of this study suggest that
species evenness enhances community productivity but
provides no benefit to invasion resistance in functionally diverse communities. However, additional studies
are needed to determine whether the effect of evenness
on invasion resistance is contingent upon the functional
diversity of the invaded community as well as the traits
of both the resident and invading species.
Acknowledgements We thank J. Alers-Garcia, A. Bennett, A.
Hartley, T. Rajaniemi, K. Rogers and K. Vogelsang for
assistance in the greenhouse. D. Campbell, J. Leichter, J.
Lemon and M. O’Connor provided outstanding greenhouse
support.
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