ORIGINAL PAPER

Competition, legacy, and priority and the success of threeinvasive species

Lora B. Perkins • Gary Hatfield

Received: 5 December 2013 / Accepted: 19 March 2014

� Springer International Publishing Switzerland 2014

Abstract Competitive ability, the ability to generate

legacy effects, and the potential to benefit from

priority, individually or interactively, are traits that

may increase the invasive potential of plants. In this

project we examine these three traits in three invasive

species (Agropyron cristatum, Bromus tectorum, and

Taeniatherum caput-medusae). Specifically in this

study, we examine competitive effects of these

invasive species, the ability of these invasive species

to generate legacy effects (as plant–soil feedback), and

the potential of these three species benefit from

priority (being sown concurrently, 30 days before,

and 30 days after the restoration species) in a green-

house study using field collected soil. Our results

suggest that all three invasive species can benefit from

priority and all three have high competitive ability.

However, only A. cristatum benefited from legacy

effects of plant–soil feedback.

Keywords Invasion syndrome � Plant–soil

feedback � Phenological niche separation �Bromus � Agropyron � Taeniatherum

Introduction

Arguments have been made that biological species

invasion is both unpredictable and idiosyncratic,

however by examining multiple traits and multiple

species simultaneously, advances in understanding

and predicting invasion can be made (Moles et al.

2012). This argument may be derived from the lack of

simple, single factor explanations for the success of

invasive species. Many individual traits have been

identified that may contribute to invasive potential of

species in select invasions and examining these in

concert will clarify what mechanisms lead to invasion

(Radford et al. 2009). Increased understanding of the

dynamics of invasion can be gained from comprehen-

sive information on the combination of traits that

contribute to invasion (Kueffer et al. 2013). This

project examines the relative importance of three of

these traits (competitive ability, legacy effects, and

priority) as mechanisms for the success of three

invasive species.

Competitive ability has long been hypothesized to

contribute to the success of invasive species (Elton

1958; Baker 1974). Though contradictory evidence

exist for this hypothesis (Vila and Weiner 2004), there

are many examples in which an invasive species is a

stronger competitor for limiting resources (i.e. has a

larger competitive interference ability, Hart and

Marshall 2012, or has a large competitive effect,

Goldberg and Landa 1991) than native species. For

example, in its invaded range Bromus tectorum has

L. B. Perkins (&)

Department of Natural Resource Management, South

Dakota State University, Brookings, SD 57007, USA

e-mail: perkinslb@gmail.com

G. Hatfield

Department of Mathematics and Statistics, South Dakota

State University, Brookings, SD 57007, USA

123

Biol Invasions

DOI 10.1007/s10530-014-0684-3

been observed to significantly decrease native species

establishment, relative growth rate, and yield, but not

be substantially impacted by natives in return (Hum-

phrey and Schupp 2004; Blank 2010). Competition

from invasive species Taeniatherum caput-medusae

reduced native grass biomass more than 60 % com-

pared to the native growing with other natives (Blank

2010).

Plants can generate legacy effects or ‘‘persistent

impacts of ecological interactions’’ (Cuddington

2011) through a variety of biotic and abiotic mecha-

nisms. Legacy effects of invasive plants have been

observed in the soil seed bank (Jurand et al. 2013),

direct and indirect effects of aboveground litter

accumulations (Vaccaro et al. 2009; Meisner et al.

2012), trait shifts in remnant native plants (Goergen

et al. 2011), in alteration of the soil microbial

community (Jordan et al. 2012; Tanner and Gange

2013), and in soil nutrient conditions (Perkins and

Nowak 2013a). These legacy effects can be generated

in as little as one growing season (Grman and Suding

2010; Perkins and Nowak 2013a) and can last for

decades (Morris et al. 2011). Plant–soil feedback

(PSF), or the alteration of soil conditions in a manner

that impact subsequent plant performance, is one type

of legacy effect that can increase individual perfor-

mance, competitive ability, population growth, and

thus, invasive potential (Cuddington and Hastings

2004; Bever et al. 2010; Perkins and Nowak 2013a, b).

For example, invader Agropyron cristatum has been

observed to alter soil nutrient availability and micro-

bial community dynamics (Jordan et al. 2012; Perkins

and Nowak 2013a) and create a PSF that increases its

own performance (Perkins and Nowak 2013b).

Differences in timing of plant growth among

species can have significant impacts on community

dynamics and invasion (Wolkovich and Cleland

2011). Invasive plants active during times of the year

when natives are not active might benefit from a

‘vacant phenological niche’, ‘phenological niche

separation’ (Wolkovich and Cleland 2011; Wain-

wright et al. 2012), or simply, invasive plants that are

active before native plants may benefit from ‘priority’

(Grman and Suding 2010). Plants that become active

earlier than other species in their community may gain

advantage by pre-emptively accessing resources

(DeFalco et al. 2007), generating asymmetric compe-

tition (Schwinning and Weiner 1998), altering flower-

pollinator synchrony (Dante et al. 2013), and thus

benefit from priority effects (Wolkovich and Cleland

2011) or seasonal priority advantage (Wainwright

et al. 2012). For example, cool season annual grass

Bromus tectorum recruits in both fall and spring

(Mack and Pyke 1983) and is a successful invader in

systems where native vegetation becomes active in

late spring (Stewart and Hull 1949). Invader B.

tectorum may benefit from a seasonal priority advan-

tage due to growth earlier in the season compared to

natives (Peterson 2005) and is able to uptake resources

before other species are active (Bilbrough and Cald-

well 1997; DeFalco et al. 2007).

Although a plant may need only one of these

mechanisms to become invasive (Perkins and Nowak

2013c), we hypothesize that successful invaders may

benefit from a combination of these traits. A plant

could have high competitive ability, benefit from

generating plant–soil feedbacks, and grow earlier than

other species. This project is designed to investigate

the importance of competitive ability, legacy effect (in

the form of plant–soil feedbacks), and priority effects

to the success of three invasive species found in the

western United States, Agropyron cristatum, Bromus

tectorum, and Taeniatherum caput-medusae. Previous

research suggests that: A. cristatum may benefit from

PSF creation (Jordan et al. 2012) more than compet-

itive ability (Francis and Pyke 1996; Perkins and

Nowak 2013b) or priority effects (Bilbrough and

Caldwell 1997); B. tectorum does not benefit from

plant soil feedbacks (Perkins and Nowak 2013a), is a

strong competitor (Humphrey and Schupp 2004;

Blank 2010; Perkins and Nowak 2013b), and might

benefit from a seasonal priority effect (Bilbrough and

Caldwell 1997; Peterson 2005); and finally, T. caput-

medusae might benefit from plant–soil feedbacks

(Perkins and Nowak 2013a), and competitive ability

(Clausnitzer et al. 1999; Blank 2010), but not priority

effects (Bilbrough and Caldwell 1997). Our hypoth-

eses are directly taken from this previous research.

Methods

A manipulative experiment was conducted in a

glasshouse in Reno, NV, USA to evaluate competi-

tion, legacy, and priority effects of three invasive

species (Agropyron cristatum, Bromus tectorum, and

Taeniatherum caput-medusae). Glasshouse conditions

were set to mimic spring field conditions with

L. B. Perkins, G. Hatfield

123

temperature range 10–20 �C and ambient light. Five

liter pots (CP512 Treepots, Steuwe and Sons, Corval-

lis OR) were used. Throughout the experiment, careful

and attentive watering kept the pots near field

capacity, which is typical of cool season precipitation

patterns in invaded areas. The experiment was initi-

ated in April 2011.

To examine competitive ability of the invasive

species, a restoration seed mix was grown with and

without seeds of the invasive species. The restoration

seed mix contained Achillea millefolium, Elymus

multisetus, Ericameria nauseosa, and Poa secunda.

Twelve seeds of each of species were planted per pot.

To examine legacy effects (as plant–soil feedbacks)

the experiment was conducted in soils collected from

field sites where the invasive species occur. The

ecosystem where soil collections were made is a semi-

arid shrubland with substantial unvegetated interspace

areas. At each field site, soil was collected from 2

immediately adjacent (within 1 m) areas from under

invader populations and from unvegetated interspace.

Soil collected from under the invader was used to

examine whether each species created a legacy effect

through plant–soil feedbacks compared to the soil

collected from non-invaded interspace areas that

represent natural ambient background soil conditions.

For each species, soil was collected from a minimum

of five paired adjacent areas and composited into

‘legacy’ and ‘ambient’ soil samples. Immediately after

collection, soil was transported back to the glasshouse

and potted.

To examine the influence of priority effects, seeds

of invaders and natives were planted concurrently or

sequentially. In pots without priority, both the resto-

ration species and the invasive species were planted at

the same time. In pots with restoration species priority,

the restoration seeds were planted 30 days before the

invasive species, and in pots with invasive priority, the

invasive species were planted 30 days before the

restoration seed. All competition treatments were

allowed to grow for 80 days after all species were

planted.

The experimental design (Fig. 1) consisted of

restoration species growing alone, restoration species

and invasives growing without priority, restoration

species and invasives growing with restoration species

given priority, and restoration species and invasives

growing with invasive species given priority either.

All these combinations were grown either in legacy

soil or in ambient soil. Each invasive species were

only grown in soils that they conditioned (their own

legacy soil) and the nearby ambient soil. In other

words, A. cristatum was only grown in soil collected

from under A. cristatum stands and nearby ambient

soil and not in soil collected from B. tectorum stands

nor the ambient soil collected from close to the B.

tectorum stands. 8 pots per invasive species were

needed for each replicate (4 competition/priority

treatments 9 2 soil legacy treatments), resulting in

24 pots (8 pots 9 3 invasive species) per replicate.

The replication level was 9.

At the end of the experiment all aboveground

biomass was collected, separated into ‘invader’,

‘restoration forb’, or ‘restoration grass’, dried for

[24 h at 60 �C, and weighed. Plant weights were used

to calculate a relative response index (RR). The RR

index is an adaptation of the RI index which has strong

mathematical and statistical properties (i.e., it is

symmetrical around zero, is linear, and has no

discontinuities in its range Armas et al. 2004; Brink-

man et al. 2010). RR allows comparison of the

restoration species performance with and without the

invasive species present controlling for differences in

soil type and overall plant size. RR was calculated

using the following formula: RR = ((bc) - (bu))/

((bc) ? (bu)) where bc is the biomass produced by

the restoration species with invaders present and bu is

the mean biomass produced by the restoration species

without invaders present. RR was calculated sepa-

rately for each of the three priority effect treatments in

ambient and legacy soil.

Data were analyzed with JMP Pro 10 (JMP Pro,

Version 10. SAS Institute Inc., Cary, NC, 2012).

Preliminary data analyses included boxplots to check

for outliers and the Box-Cox Y Transformation to

examine possible power transformations that would be

best in terms of satisfying the usual regression

assumptions of normality and homogeneity of vari-

ance (no data were excluded and no transformations

were necessary). Restoration grass and forb biomass

was combined to evaluate the cumulative effect on

restoration species performance. Multivariate regres-

sion analysis was used to examine the effect of soil

conditioning, competition, priority, and the interaction

of soil conditioning and competition on four responses

for each species. Mutually orthogonal contrasts were

used to answer specific research questions and min-

imize the potential for Type I error.

Success of three invasive species

123

Results

Agropyron cristatum

The biomass of restoration plants (forbs ? grasses)

(Fig. 2a) was highest when grown without A. cristatum

in legacy soil (mean biomass = 1.88 g, se = 0.21)

and lowest when grown in legacy soil where the

invader had priority (mean biomass = 0.11 g,

se = 0.05; a 94 % reduction in biomass). Restoration

plant biomass (Fig. 2a) was significantly affected by

competition (F1,49 = 47.61, p = \0.001), and by an

interaction of competition and legacy (F3,49 = 3.93,

p = 0.01), although the main effect of legacy was not

significant (F3,49 = 2.60, p = 0.11). Priority also

significantly affected the biomass produced by resto-

ration plants (F1,49 = 94.60, p = \0.001) with signif-

icantly less biomass produced (over a 90 % decrease)

when the invader had priority, but no significant

difference between pots where restoration plants had

priority and pots where both invasive species and

restoration plants were sown concurrently (Fig. 2a).

The relative response (RR) of the restoration plants

(Fig. 3a) was significantly affected by competition

(F1,39 = 61.83, p = \0.001), legacy (F2,39 = 26.11,

p = \0.001), and the interaction of competition and

legacy (F2,39 = 3.25, p = 0.0496). Priority also sig-

nificantly affected RR (F1,39 = 137.85 p = \0.001).

Bromus tectorum

The biomass of restoration plants (forbs ? grasses) was

highest when grown without B. tectorum in ambient soil

(mean biomass = 1.40 g, se = 0.08) and lowest when

grown in pots where B. tectorum had priority in legacy

soil (mean biomass = 0.007 g, se = 0.0003; over a

99 % decrease in biomass). The biomass of restoration

plants (Fig. 2b) was significantly affected by competi-

tion (F3,58 = 161.17, p = \0.001) with B. tectorum, but

not legacy (F1,58 = 3.26, p = 0.076) nor by the inter-

action of competition and legacy (F3,58 = 1.42,

p = 0.25). Priority also significantly affected the bio-

mass produced by restoration plants (F1,58 = 387.99,

p = \0.001). The relative response (RR) of restoration

plants (Fig. 3b) was significantly affected by competi-

tion (F2,48 = 87.44, p = \0.001), legacy (F1,48 = 8.72,

p = 0.0049), but not the interaction of competition and

legacy (F2,48 = 3.10, p = 0.054). Priority also signifi-

cantly affected RR (F1,48 = 415.29 p = \0.001) with

significantly less biomass produced by the restoration

species when B. tectorum had priority compared to

when the restoration species had priority (Fig. 3b).

Taeniatherum caput-medusae

The biomass of restoration plants (Fig. 2c) was highest

when grown without T. caput-medusae in ambient soil

Fig. 1 Experimental design used to examine three traits

[competitive ability, legacy (as plant–soil feedback creation)],

and priority for the success of three invasive species.

Competitive ability is determined with comparison of the

performance of restoration species with and without an invader.

Legacy is determined by comparison of performance in

conditioned and ambient soil. Priority is determined by

comparison of performance among pots were the restoration

species and the invasive species were sown concurrently, pots

where the natives were sown first, and pots were the invader was

sown first

L. B. Perkins, G. Hatfield

123

(mean biomass = 0.51 g, se = 0.06) and lowest when

grown in pots where the invader had priority in ambient

soil (mean biomass = 0.02 g, se = 0.006; a 96 %

decrease in biomass). The biomass of restoration plants

was significantly affected by competition (F3,63 =

51.99, p = \0.001), but not legacy (F1,63 = 0.76,

p = 0.39) nor by the interaction of competition and

legacy (F3,63 = 1.84, p = 0.15). Priority also signifi-

cantly affected the biomass produced by restoration

plants (F1,63 = 120.89, p = \0.001). The relative

response (RR) of the restoration plants (Fig. 3c) was

significantly affected by competition (F2,46 = 48.25,

p = \0.001) and legacy (F1,46 = 6.31, p = 0.016),

but not the interaction of competition and legacy

(F2,46 = 0.56, p = 0.57). Priority also significantly

affected RR (F1,46 = 272.58, p = \0.001).

Our results indicate that A. cristatum has a signif-

icant competitive effect (indicated by negative RR

values), benefits from legacy effects (represented by

lower RR values in legacy soil compared to ambient

soil), and from priority (indicated by significantly

lower RR values in the invader first priority treat-

ment). Further, our results indicate that B. tectorum

has a significant competitive effect (indicated by RR

values near -1 which indicate near competitive

exclusion of the restoration plants), does not benefit

from legacy effects (represented by lower RR values

in ambient soil compared to legacy soil), and does

benefit from priority (indicated by significantly lower

RR values in the invader first priority treatment).

Finally, our results indicate that T. caput-medusae has

a significant competitive effect (indicated by negative

RR values with some RR values near -1 which

indicate near competitive exclusion of the restoration

plants), does not benefit from legacy effects (repre-

sented by no significant differences between RR

Fig. 2 Biomass the restoration species produced in either

ambient or the invasive species legacy soil. Restoration species

were either sown alone (no invader), earlier than the invader

(restoration spp first), at the same time as the invader

(concurrent), or after the invader (invader first)

Fig. 3 The relative response of the restoration species to

competition. A value of zero would indicate that the presence of

the invasive species did not affect biomass produced; a negative

value (maximum = -1) indicates less restoration species

biomass was produced in pots where invasive species were

present

Success of three invasive species

123

values in legacy soil compared and ambient soil), and

does benefit from priority (indicated by significantly

lower RR values in the invader first priority

treatment).

Discussion

The results of our research investigating the contribu-

tion of three traits: competitive ability, legacy effects

(as plant–soil feedback creation), and priority effects

to the invasiveness of three invasive species (A.

cristatum, B. tectorum, and T. caput-medusae) suggest

that competitive ability may be the dominant trait

contributing to two invasive species (B. tectorum and

T. caput-medusae) success and that A. cristatum may

benefit from all three traits. Although, priority effects

did benefit all three invasive species (see discussion

below), when restoration plants and invasive species

were grown concurrently (without priority), all three

invasive species demonstrated substantial competitive

effects. This result suggests that although these

invasive species can benefit from priority, it is not

required for their success in their invaded ranges. A.

cristatum was the only species that benefited from

legacy effects.

All three of the invasive species studied generated

large competitive effects on restoration species bio-

mass in all three priority treatments. Two species, B.

tectorum and T. caput-medusae nearly competitively

excluded restoration species. This result is a higher

than the average loss of native biomass (46.6 %)

reported in meta-analysis (Vila and Weiner 2004), but

is consistent with the high density and near monotypic

stands these three invaders have been reported to

create in the field (Young and Evans 1973; Davies and

Svejcar 2008; Davies et al. 2013).

In this study, only one species (A. cristatum, not B.

tectorum nor T. caput-medusae) benefited from legacy

effects measured as plant–soil feedback. Plant–soil

feedbacks have been observed to effect both subse-

quent plant growth and competitive interactions. Of

the five plant–soil feedback types possible, only two

potentially contribute to invasiveness (Perkins and

Nowak 2013a). These two types are either a hetero-

specific negative feedback wherein all subsequent

plant growth is decreased due to soil conditioning by

the invasive species but other species are more

strongly affected than the invader, or a conspecific

positive feedback wherein all subsequent plant per-

formance is enhanced due to soil conditioning with the

invasive species incurring the largest benefit (Perkins

and Nowak 2013a). Meta-analysis suggests that most

species do not benefit from plant–soil feedbacks and

that perennials incur less negative effects of PSF than

annuals (Kulmatiski et al. 2008). Our results agree

with both of these observations in that that the species

that benefited was the perennial grass and the two that

did not benefit from PSF were annual grasses.

Our results that A. cristatum impacted restoration

plant performance more in its own soil than in ambient

soil agree with previous research. In a greenhouse

study, A. cristatum legacy soil has been observed to

decrease growth of native forbs (Jordan et al. 2008)

and increase conspecific competitive ability (Perkins

and Nowak 2013b). The PSF generated by A. crista-

tum may be due to alteration of arbuscular-mycorrhi-

zal fungi (Jordan et al. 2012) or soil nutrient

availability (Perkins and Nowak 2013a). Restoration

of areas occupied by A. cristatum has a high probably

of failure (Davies et al. 2013), to which the legacy

effect of the plant–soil feedback may contribute.

Previous work has indicated that T. caput-medusae

has the ability to create plant–soil feedbacks that may

increase its invasive potential (Perkins and Nowak

2013a). T. caput-medusae has been observed to create

a heterospecific negative PSF type wherein all species

performance was reduced in legacy soil and other

species were more strongly impacted than T. caput-

medusae (Perkins and Nowak 2013a). This PSF

phenomenon may still be seen in the results presented

here (Fig. 2c, restoration species grown with no

invader) although among all the competition and

priority treatments, legacy did not significantly affect

restoration species biomass. It is possible that T.

caput-medusae has high competitive ability and can

generate plant–soil feedbacks, but when compared

together PSF effect is small compared to the large

effect of competitive ability. In other words, even if a

heterospecific negative PSF was created (restoration

plants performed worse in T. caput-medusae legacy

soil than in the ambient soil, Fig. 2c), the impact of the

PSF was small enough to be overwhelmed by the large

competitive effect of T. caput-medusae. These results

may have two implications. During invasion or when

T. caput-medusae is present at a site, competitive

ability may be the trait contributing to its success.

However, when T. caput-medusae is removed from a

L. B. Perkins, G. Hatfield

123

site, plant–soil feedbacks may need to be addressed to

facilitate restoration of native species.

Our results suggest three species have the potential

to benefit from priority effects, as is observed in other

research (Grman and Suding 2010; Dickson et al. 2012;

Wainwright et al. 2012). This is not a surprising result

considering our intentional creation of the priority

effect as a treatment in the greenhouse. In the field, B.

tectorum does become active before co-occuring

natives (Stewart and Hull 1949; Peterson 2005). This

result can be interpreted as the potential for A.

cristatum and T. caput-medusae to create larger effects

on restoration species if they germinate and establish

first in the field. This experiment was conducted in the

greenhouse which allowed for precise environmental

control, but result should not be interpreted as evidence

that all invasive species absolutely benefit from

priority, legacy, or competition on the landscape under

field conditions. An appropriate method to determine

the importance of these factors to these invasive

species success would be to observe phenology and the

timing of growth of invasive species versus restoration

species in a natural setting.

Invasion syndromes suggest that different traits

may contribute to invasion depending on the charac-

teristics of the potentially invaded site (Perkins and

Nowak 2013c). The three traits examined in this

experiment have been hypothesized to be beneficial

for an invader in disparate environments (Perkins and

Nowak 2013a, b, c). Competitive ability has been

hypothesized to be beneficial in environments with

high resource availability (i.e. less stressful environ-

ments). Plant–soil feedback creation has been hypoth-

esized to be beneficial in environments with low

resource availability (i.e. more stressful environ-

ments). Priority effects or phenological niche separa-

tion might be beneficial regardless of environmental

conditions (Perkins and Nowak 2013c). All three of

our study species are successful invasive species in the

Great Basin region of western North America. Gen-

erally, the Great Basin is a cold desert climate type

with most precipitation falling in the winter. Initially,

this would seem to be a low resource environment and

thus plant–soil feedback creation and not competitive

ability would be hypothesized (based on invasion

syndromes, Perkins and Nowak 2013c) to be a trait

that contributes to invasive potential in this environ-

ment. However, B. tectorum and T. caput-medusae are

both cool season annual grasses that are active early in

the season when soil moisture is still available. Having

high competitive ability may be advantageous for

species active early in the season when resources are

not limited. A. cristatum is a cool-season perennial

grass. Competitive ability may be advantageous for A.

cristatum early in the season (similar to B. tectorum

and T. caput-medusae). But as a perennial, A. crist-

atum needs to persist year-round and perhaps being

able to generate beneficial plant–soil feedbacks is

advantageous during more stressful times of the year.

These results agree with others in suggesting that

invasion depends on unique and identifiable combi-

nations of environmental conditions and species traits

(Moles et al. 2012; Radford 2013). Increased exam-

ination and consideration of these, or similar, invasion

syndromes (or recurrent associations of species trait X

environment relationships, Kueffer et al. 2013) will

advance theoretical development of the discipline.

Identification and testing potential invasion syn-

dromes represents advancement in the field of inva-

sion science (Kueffer et al. 2013). It is reasonable to

consider that certain traits that allow a species to

become invasive in a site with certain conditions may

enable other species with the same traits to become

invasive in other sites with similar conditions (Perkins

and Nowak 2013c). Examination of the relationship of

the traits that contribute to species invasiveness with

habitat characteristics is a research strategy that will

build on the strengths of past invasion science and

improve understanding of biological invasion dynam-

ics and will provide better information for land

management (Kueffer et al. 2013).

Acknowledgments This work was supported by the South

Dakota Agricultural Experiment Station and the Nevada

Agricultural Experiment Station. The manuscript was

improved by comments and suggestions of anonymous

reviewers and Dr. KC Jensen.

References

Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant inter-

actions: a new comparative index. Ecology 85:2682–2686

Baker H (1974) The evolution of weeds. Annu Rev Ecol Syst

5:1–24

Bever JD, Dickie IA, Facelli E et al (2010) Rooting theories of

plant community ecology in microbial interactions. Trends

Ecol Evol 25:468–478

Bilbrough CJ, Caldwell MM (1997) Exploitation of springtime

ephemeral N pulses by six great basin plant species.

Ecology 78:231–243

Success of three invasive species

123

Blank RR (2010) Intraspecific and interspecific pair-wise seedling

competition between exotic annual grasses and native

perennials: plant–soil relationships. Plant Soil 326:331–343

Brinkman EP, Van der Putten WH, Bakker EJ et al (2010) Plant–

soil feedback: experimental approaches, statistical analy-

ses and ecological interpretations. J Ecol 98:1063–1073

Clausnitzer DW, Borman MM, Johnson DE (1999) Competition

between Elymus elymoides and Taeniatherum caput-

medusae. Weed Sci 47:720–728

Cuddington K (2011) Legacy effects: the persistent impact of

ecological interactions. Biol Theory 6:203–210

Cuddington K, Hastings A (2004) Invasive engineers. Ecol

Model 178:335–347

Dante SK, Schamp BS, Aarssen LW (2013) Evidence of

deterministic assembly according to flowering time in an

old-field plant community. Funct Ecol 27:555–564

Davies KW, Svejcar TJ (2008) Comparison of medusahead-

invaded and noninvaded Wyoming big sagebrush steppe in

southeastern Oregon. Rangel Ecol Manag 61:623–629

Davies KW, Boyd C, Nafus A (2013) Restoring the sagebrush

component in crested wheatgrass-dominated communities.

Rangel Ecol Manag 66(4):472–478

DeFalco LA, Fernandez GCJ, Nowak RS (2007) Variation in the

establishment of a non-native annual grass influences

competitive interactions with Mojave Desert perennials.

Biol Invasions 9:293–307

Dickson TL, Hopwood JL, Wilsey BJ (2012) Do priority effects

benefit invasive plants more than native plants? An experi-

ment with six grassland species. Biol Invasions 14:2617–2624

Elton C (1958) The ecology of invasions by animals and plants.

University of Chicago Press, Chicago

Francis MG, Pyke DA (1996) Crested wheatgrass cheatgrass

seedling competition in a mixed-density design. J Range

Manag 49:432–438

Goergen EM, Leger EA, Espeland EK (2011) Native perennial

grasses show evolutionary response to Bromus tectorum

(Cheatgrass) invasion. PLoS One 6:e18145

Goldberg DE, Landa K (1991) Competitive effect and response:

hierarchies and correlated traits in the early stages of

competition. J Ecol 79:1013–1030

Grman E, Suding KN (2010) Within-year soil legacies contribute

to strong priority effects of exotics on native California

grassland communities. Restor Ecol 18:664–670

Hart SP, Marshall DJ (2012) Advantages and disadvantages of

interference-competitive ability and resource-use effi-

ciency when invading established communities. Oikos

121:396–402

Humphrey LD, Schupp EW (2004) Competition as a barrier to

establishment of a native perennial grass (Elymus elymo-

ides) in alien annual grass (Bromus tectorum) communi-

ties. J Arid Environ 58:405–422

Jordan NR, Larson DL, Huerd SC (2008) Soil modification by

invasive plants: effects on native and invasive species of

mixed-grass prairies. Biol Invasions 10:177–190

Jordan NR, Aldrich Wolfe L, Huerd SC et al (2012) Soil-

occupancy effects of invasive and native grassland plant

species on composition and diversity of mycorrhizal

associations. Invasive Plant Sci Manag 5:494–505

Jurand BS, Abella SR, Suazo AA (2013) Soil seed bank lon-

gevity of the exotic annual grass Bromus rubens in the

Mojave Desert, USA. J Arid Environ 94:68–75

Kueffer C, Pysek P, Richardson DM (2013) Integrative invasion

science: model systems, multi-site studies, focused meta-

analysis and invasion syndromes. New Phytol 200:615–633

Kulmatiski A, Beard KH, Stevens JR et al (2008) Plant–soil

feedbacks: a meta-analytical review. Ecol Lett 11:980–992

Mack RN, Pyke DA (1983) The demography of Bromus tecto-

rum: variation in time and space. J Ecol 71:69–93

Meisner A, de Boer W, Cornelissen JHC et al (2012) Reciprocal

effects of litter from exotic and congeneric native plant

species via soil nutrients. PLoS One 7:8

Moles AT, Flores-Moreno H, Bonser SP et al (2012) Invasions:

the trail behind, the path ahead, and a test of a disturbing

idea. J Ecol 100:116–127

Morris LR, Monaco TA, Sheley RL (2011) Land-use legacies and

vegetation recovery 90 years after cultivation in great basin

sagebrush ecosystems. Rangel Ecol Manag 64:488–497

Perkins LB, Nowak RS (2013a) Native and non-native grasses

generate common types of plant–soil feedbacks by altering

soil nutrients and microbial communities. Oikos 122:

199–208

Perkins LB, Nowak RS (2013b) Soil conditioning and plant–soil

feedbacks affect competitive relationships between native

and invasive grasses. Plant Ecol 213:1337–1344

Perkins LB, Nowak RS (2013c) Invasion syndromes: hypothe-

ses on relationships among invasive species attributes and

characteristics of invaded sites. J Arid Land 5:275–283

Peterson EB (2005) Estimating cover of an invasive grass

(Bromus tectorum) using tobit regression and phenology

derived from two dates of Landsat ETM plus data. Int J

Remote Sens 26:2491–2507

Radford IJ (2013) Fluctuating resources, disturbance and plant

strategies: diverse mechanisms underlying plant invasions.

J Arid Land 5:284–297

Radford IJ, Dickinson KJM, Lord JM (2009) Does disturbance,

competition or resource limitation underlie Hieracium

lepidulum invasion in New Zealand? Mechanisms of estab-

lishment and persistence, and functional differentiation

among invasive and native species. Aust Ecol 35:282–293

Schwinning S, Weiner J (1998) Mechanisms determining the

degree of size asymmetry in competition among plants.

Oecologia 113:447–455

Stewart G, Hull AC (1949) Cheatgrass (Bromus tectorum L.): an

ecologic intruder in Southern Idaho. Ecology 30:58–74

Tanner RA, Gange AC (2013) The impact of two non-native

plant species on native flora performance: potential impli-

cations for habitat restoration. Plant Ecol 214:423–432

Vaccaro LE, Bedford BL, Johnston CA (2009) Litter accumulation

promotes dominance of invasive species of cattails (Typha

spp.) in Lake Ontario wetlands. Wetlands 29:1036–1048

Vila M, Weiner J (2004) Are invasive plant species better

competitors than native plant species? Evidence from pair-

wise experiments. Oikos 105:229–238

Wainwright CE, Wolkovich EM, Cleland EE (2012) Seasonal

priority effects: implications for invasion and restoration in

a semi-arid system. J Appl Ecol 49:234–241

Wolkovich EM, Cleland EE (2011) The phenology of plant

invasions: a community ecology perspective. Front Ecol

Environ 9:287–294

Young JA, Evans RA (1973) Downy brome: intruder in the plant

succession of big sagebrush communities in the Great

Basin. J Range Manag 26:410–415

L. B. Perkins, G. Hatfield

123