Ecological correlates of invasion by Arundo donax in three southern California riparian habitats

ORIGINAL PAPER

Ecological correlates of invasion by Arundo donax in threesouthern California riparian habitats

Lauren D. Quinn Æ Jodie S. Holt

Received: 28 November 2006 / Accepted: 10 August 2007 / Published online: 5 September 2007

� Springer Science+Business Media B.V. 2007

Abstract Arundo donax L. (Poaceae) is an aggres-

sive invader in California’s riparian habitats. Field

experiments were conducted to examine invader and

site attributes important in early invasion. One

hundred A. donax rhizomes were planted along five

transects into each of three southern California

riparian habitats. Pre-planting rhizome weight was

recorded, along with site variables including percent

bare ground, litter depth, PAR, soil moisture, soil

temperature, incidence of herbivory, native canopy

cover, and plant community richness and diversity.

A. donax shoot emergence, survival time, and shoot

height were recorded for approximately 10 months.

The experiment was repeated over three years in

different locations within each site. When years and

sites were pooled to reveal large-scale patterns,

A. donax performance was explained by rhizome

weight, soil moisture, bare ground, soil temperature,

and herbivory. When each site was considered singly,

A. donax was positively correlated with different

variables in each location. Species richness was

correlated with A. donax performance in only one

site. Our results indicate that A. donax establishment

in riparian habitats is promoted by both vegetative

reproduction and favorable abiotic environmental

factors and relatively unaffected by the composition

of the native community. The positive response of

A. donax to disturbance (bare ground) and high

resource availability (soil moisture), combined with

a competitive perennial habit suggest that this species

takes advantage of a competitive-ruderal life history.

The ability of A. donax to respond to different

conditions in each site combined with low genetic

and phenotypic variation seen in other studies also

suggests that a high degree of environmental toler-

ance contributes to invasion success.

Keywords Arundo donax � Ecological correlates �Invasibility � Riparian � Vegetative reproduction

Introduction

Arundo donax L. (Poaceae) is a non-native plant that

has invaded California’s riparian systems since its

introduction from the Mediterranean region in the

early 1800’s (Dudley 2000). Large established clones

spread belowground by extension of robust rhizomes,

even into surrounding competitive environments

(Quinn et al. 2007), and disperse downstream by

rhizomes that are dislodged during flood events.

Among its many negative impacts on riparian eco-

systems are the increased frequency of destructive

L. D. Quinn

CSIRO Entomology, 120 Meiers Rd, Indooroopilly,

QLD 4068, Australia

e-mail: lauren.quinn@csiro.au

J. S. Holt (&)

Department of Botany and Plant Sciences, University

of California, Riverside, CA 92521, USA

e-mail: jodie.holt@ucr.edu

123

Biol Invasions (2008) 10:591–601

DOI 10.1007/s10530-007-9155-4

fires, removal of soil water supplies, destruction of

bridges and culverts during floods, and degradation of

habitat for native birds and other fauna (Bell 1997).

Despite management concerns and the millions of

dollars that have been spent to control this species

(OCWD 2004), few studies have characterized its

basic biology or the ecological processes that

contribute to its apparent success at the earliest

stages of establishment.

Many invasion biologists have focused on identi-

fying the physiological or morphological attributes

contributing to invasiveness, while others have stud-

ied environmental and community characteristics that

favor invasion by non-natives. Several attributes have

been shown to be common to many invasive plants

(Baker 1974; Mack 1996). Studies that focused on

predominantly seed-producing species found small

seed mass, short juvenile period, and high specific

leaf area to be important in invasion (Rejmanek and

Richardson 1996; Hamilton et al. 2005), while veg-

etative reproduction has been correlated with

invasiveness for several rhizomatous species (Kolar

and Lodge 2001; Lloret et al. 2005), including

A. donax (Quinn 2006). Such traits may confer

advantages to invasive species, but all plants are

constrained to some extent by their physiological

tolerance to environmental conditions.

Environmental factors are of paramount impor-

tance to plant establishment and can vary widely even

within a specific habitat type. Thus, the local

distribution of invasive plants can be highly depen-

dent on these factors (Crawley 2003). For example,

the extent of A. donax spread has been correlated

with nitrogen availability (Quinn et al. 2007) and

varies markedly between two southern California

field sites that receive different quantities of nitrog-

enous effluent, even though the two sites lie less than

72 km apart (Decruyenaere and Holt 2005). Nitrogen

availability has been implicated in invasibility by

many authors (Stohlgren et al. 1999; Fenn et al.

2003; Huston 2004; Blumenthal 2006), but this

represents only one environmental variable that

influences invasions. Depending on the species being

studied, other important abiotic factors include dis-

turbance (Hobbs and Huenneke 1992; Burke and

Grime 1996), soil moisture (Meekins and McCarthy

2001), temperature (Beerling 1993), radiation (Myers

et al. 2005; Caplan and Yeakley 2006), and many

others.

The biotic environment, specifically native plant

community properties, can also influence invasive

plant success. Native plant communities have been

described as either resistant or susceptible to invasion

based on species diversity (Elton 1958; Stohlgren

et al. 1999; Naeem et al. 2000; Kennedy et al. 2002;

Levine et al. 2003) and on native plant identity

(Prieur-Richard et al. 2002; Dodd et al. 2004). At the

local scale, native species diversity often correlates

with invasion resistance (Levine 2000). In some

cases, the negative effects of community properties

on invaders may not be strong enough to prevent

initial establishment, but can constrain the abundance

of invaders once they have established (Levine et al.

2004).

Because the success of A. donax has in part been

attributed to both plant traits and habitat conditions

(Boose and Holt 1999; Khudamrongsawat et al.

2004; Decruyenaere and Holt 2005; Quinn et al.

2007), an integrative approach that investigates these

factors and their interactions should provide a more

mechanistic understanding of the invasion process

than studying either factor alone and may permit

more specific management recommendations to be

made. In this research, an experiment was conducted

to examine factors responsible for early establishment

of A. donax in southern California riparian systems

by asking whether A. donax success was influenced

by (1) rhizome characteristics at the initial establish-

ment phase, (2) environmental factors measured in

three riparian habitats, and (3) richness and diversity

of the surrounding native community.

Materials and methods

Site descriptions

Three southern California watersheds were selected

in winter 2003. All three sites were moderately to

heavily invaded by mature A. donax, but portions of

the native riparian community remained intact.

Dominant native species included Salix lasiolepis,

S. gooddingii, Populus fremontii, Platanus racemosa,

and Baccharis salicifolia. The Riverside (RIV) site

(33� 58.121 N, 117� 26.105 W) was located along

the Santa Ana River in Riverside, in Riverside

County, CA; the San Diego (SD) site (33�15.334 N, 117� 17.471 W) was located along the

592 L. D. Quinn, J. S. Holt

123

San Luis Rey River in Oceanside, in San Diego

County, CA; the Orange County (OC) site (33�33.718 N, 117� 43.107 W) was located along Aliso

Creek in Aliso Viejo, in Orange County, CA. All

soils were classified as sandy loam (Bowman 1973;

Wachtell 1978). These sites will be referred to by

their county abbreviations as RIV, SD, and OC,

respectively.

At each site, five 25-m permanent transects were

established perpendicular to the watercourse. Tran-

sects were placed to avoid intersecting existing

A. donax clumps, and were at least 10 m and up to

30 m apart. Five 1.5 m · 0.5 m plots were centered

along each transect, randomly spaced, with the longer

side parallel to the watercourse.

Planting design

About 100 A. donax rhizome pieces were excavated

from each site in each of 3 years, on April 11, 2003,

February 13, 2004, and again on February 25, 2005

Late rainfall in the first year prevented an earlier date

for initiating the experiment. Rhizomes were brought

back to the lab to be inventoried for volume, fresh

weight, and number of buds. Prior to measurement,

rhizomes were cleaned and trimmed, and existing

shoots and roots were removed. After inventory and

cold storage (4�C) for approximately 1 week, rhi-

zomes ranging from 5 to 17 cm in length were

planted back into their respective field sites. Four

rhizomes were planted and their locations marked in

each field plot. Rhizomes were equally spaced along

the long edge of the plot. Any existing litter and

surrounding vegetation were kept intact during

planting.

The experiment was conducted over three years.

Rhizomes were planted on April 22 and 24 in 2003,

on March 1, 3, and 4 in 2004, and on March 8 and 10

in 2005. For the 2003 and 2004 plantings, new plots

were established along the same transects in all sites.

In 2005, new plots were placed along existing

transects in OC, but transects were relocated in the

SD site due to destructive flooding. In the same year,

flooding continued after planting in the RIV site, and

several plots were lost. After two replanting attempts

were thwarted by continued flooding, the RIV site

was abandoned. After finding evidence of herbivory

in all sites in 2003, herbivory exclosures

(approximately 45 cm tall · 30 cm diameter) were

constructed from ½ inch wire aviary netting and

placed around the shoots as they emerged in 2004 and

2005. In 2003, and to a lesser extent in subsequent

years, many of the new shoots were chewed to

ground level and several rhizomes appeared to have

been excavated from the ground and placed near the

original planting site. While the culprits were never

seen, we suspect, from the angle of the chewed edge,

that rabbits were responsible for eating the new

shoots and, from the general pattern of ground

disturbance nearby, that wild boars were responsible

for digging rhizomes out of the ground. On December

9 and 16 of 2005, surviving A. donax stems from the

three years of the experiment were cut and sponged

with a 75% solution of wetland-approved glyphosate

(AquaMaster�, Monsanto Corporation) and all other

materials were removed from the three sites.

Data collection

For the first 2 months after planting in all years and

sites, sites were visited weekly to monitor the date of

A. donax shoot emergence from planted rhizomes.

Thereafter, sites were visited on a biweekly basis to

record additional shoot emergence, shoot height, and

shoot senescence date. Because shoots were not

monitored for more than 1 year and a cohort of plants

from each year survived, plants that did not emerge or

senesce during the experimental period (planting

through December) each year were assigned an

emergence time or survival time of 365 days for

analysis purposes. Notations were made if evidence

of herbivory was seen, and these were later quantified

as the percent of each plot having experienced

herbivory. At the time of planting, percent bare

ground estimates were made and litter depth was

measured in three locations per plot. Monthly mea-

surements of soil volumetric water content (Campbell

HydroSense meter with 20 cm CS620 soil probes)

and soil temperature (13 cm max/min waterproof

digital thermometer, Forestry Suppliers) were

recorded in two locations per plot. PAR as percent

of full sun was recorded for each plot three times

during each year, once at planting and twice more

during the experimental period (LiCor 1000 Data-

logger and LiCor 191SA Line Quantum Sensor).

Species richness and percent cover by natives

Ecological correlates of invasion by Arundo donax 593

123

(convex spherical densiometer, Forestry Suppliers) in

each plot was determined at the time of planting. In

2004 and 2005, numbers of native individuals in each

plot were estimated using the following categories:

1–5, 6–10, 11–15, 16–20, or 25+ individuals. Cate-

gory averages were used to calculate average plot

diversity using the Shannon–Weiner index. Soil was

collected from all transects (5 per site) in autumn

2004, allowed to dry in ambient laboratory condi-

tions, ground in a coffee grinder, and sent for nitrate

and ammonium analysis at the UC Davis Division of

Agriculture and Natural Resources (DANR) analyt-

ical facility. Climate data, including precipitation,

relative humidity, and air temperature were obtained

online from the weather stations nearest to the sites.

We used station #44 at the UC Riverside campus for

our RIV site, station #62 in Temecula for our SD site,

and station #75 in Irvine for our OC site (California

Irrigation Management Information System).

Data analysis

Data were assessed for normality and subjected to

analysis of variance, analysis of covariance, and

multiple regressions to identify sources of variation in

abiotic variables and A. donax response variables.

Dependent variables represented A. donax establish-

ment and included time to emergence, height, and

survival time. A. donax response measurements for

the four rhizomes in each plot were averaged to give

a single plot value. Independent variables included

rhizome fresh weight (g), soil moisture (%) and

temperature (�C), radiation (% of full sun), bare

ground (%), litter depth (cm), percent cover (%),

native species richness (# species per plot), commu-

nity diversity (H0), and herbivory (%). When all sites

and years were pooled, the maximum number of

observations entered into analyses was 200, com-

prised of 25 plots · 2 sites · 3 years (for OC and

SD) and 25 plots · 2 years for the RIV site. When all

sites and years were pooled for analyses of variance,

n = 200 for the OC and SD sites and years 2003 and

2004, but n = 125 for the RIV site and year 2005.

Also, because diversity was not measured in 2003,

this variable was removed in analyses that pooled all

years.

One-way analyses of variance determined differ-

ences in environmental variables and A. donax

response variables between years and sites. We

employed Tukey’s HSD multiple comparison test

for pairwise comparisons between years and sites.

Analyses of covariance were used to determine the

relative contribution of all the continuous environ-

mental variables and of the categorical variables year

and site to the variance in A. donax response

variables. When sites were considered individually

over the years, multiple regression was used to assess

the influence of the independent variables on

A. donax response variables. To assess the degree

of collinearity of each independent variable, variance

inflation factors (VIF) for each variable were calcu-

lated. Collinearity is a major problem at VIF ‡ 10

(Myers 1986; Chatterjee et al. 2000), while VIF ‡ 4

indicates potential collinearity that should be inves-

tigated further (Fox 1997). While one recent paper

suggests that VIF values as low as two may indicate

collinearity (Graham 2003), independent variables

with VIF £ 4 were retained in the multiple regression

analyses presented here. In the one site where VIF

values exceeded four, one of the two collinear

variables was omitted from the analysis. Independent

variables were also tested for simple correlation using

Pearson’s product-moment correlation coefficient (r).

All analyses were performed using SYSTAT 10.0

(SPSS Inc, Point Richmond, CA).

Results

Large scale environmental patterns

According to weather station data that illustrated

large scale climate patterns, certain aspects of climate

differed between sites but not between years. Aver-

age relative humidity was lowest in RIV (F = 6.68,

P £ 0.005), while maximum air temperature was

marginally lower in OC than the two other sites

(F = 2.37, P = 0.10) (Fig. 1). Precipitation, total

radiation, and air temperature did not differ according

to site, year, or their interaction (data not shown). Soil

nitrate levels differed between sites (F = 12.27,

P £ 0.001), with RIV having greater values than SD

or OC (RIV: 4.96 ± 0.88 ppm; SD: 2.06 ± 0.29 ppm;

OC: 1.34 ± 0.19 ppm). Ammonium levels did not

differ between sites (F = 0.74, P = 0.50; RIV:

2.34 ± 0.62 ppm; SD: 2.80 ± 0.19 ppm; OC: 3.36 ±

0.80 ppm).

594 L. D. Quinn, J. S. Holt

123

Environmental conditions across sites

When years were pooled to isolate general site-

dependent patterns, most independent variables dif-

fered according to site. OC was characterized by

having relatively low soil temperature and moisture

values, low PAR values, little bare ground and native

cover, high species richness and diversity, and low

incidence of herbivory (Tables 1, 2). RIV was

characterized by having relatively high soil temper-

ature and moisture values, low PAR values, abundant

bare ground and native cover, low species richness

and diversity, and low incidence of herbivory

(Tables 1, 2). SD was characterized by having

relatively high soil temperatures and moderate soil

moisture, high PAR values, abundant bare ground

and native cover, low species richness and diversity,

and high incidence of herbivory (Tables 1, 2). Litter

depth did not vary between sites. Finally, initial

rhizome fresh weight differed according to site, with

the greatest values in RIV (Tables 1, 2).

Ecological correlates of A. donax performance

When analyses of covariance (ANCOVA) were

performed using year and site as categorical variables

and all but diversity entered as continuous environ-

mental variables (n = 200), emergence time was not

significantly explained by any of the variables

included in the model (data not shown). About 49%

of the variation in survival time was accounted for by

site (P £ 0.0001), rhizome fresh weight (P £ 0.001),

soil moisture (P £ 0.005), percent bare ground

(P £ 0.05), and herbivory (P £ 0.001) (Table 3).

About 46% of the variation in shoot height was

0

10

20

30

40

50

60

70

80

90

Apr-0

3

Jun-

03

Aug-0

3

Oct-03

Dec-0

3

Mar

-04

May

-04

Jul-0

4

Sep-0

4

Nov-0

4

Feb-0

5

Apr-0

5

Jun-

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Aug-0

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Oct-05

Dec-0

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Max

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(C

)

0102030405060708090100

Ave

rag

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ve h

um

idit

y (%

)

UCR (Tmax) UCR (RHavg) Temecula (Tmax)

Temecula (RHavg) Irvine (Tmax) Irvine (RHavg)

Fig. 1 Maximum air temperature (filled symbols) and average

relative humidity (empty symbols) values from the nearest

weather stations to the three field sites used in this three-year

experiment. UCR station was nearest to the Riverside (RIV)

site, Temecula weather station was nearest to the San Diego

(SD) site, and Irvine weather station was nearest to the Orange

County (OC) site

Table 1 Analyses of variance showing mean differences

between sites for all independent variables with years pooled

(n = 200 for OC and SD, but n = 125 for RIV, since this site

was only included in 2003 and 2004)

Independent variable Effect

of site

Pairwise comparisons

OC RIV SD

Rhizome FW P 0.0001 a b a

F 33.76

PAR P 0.0001 a b c

F 38.59

Soil temperature P 0.001 a b b

F 6.79

Soil moisture P 0.05 a b ab

F 3.21

Percent bare ground P 0.0001 a b b

F 15.55

Litter depth P NS n/a n/a n/a

F 1.11

Percent native cover P 0.0001 a b c

F 27.42

Species richness P 0.0001 a b c

F 43.35

Community diversity P 0.0001 a b b

F 28.47

Herbivory P 0.0001 a b c

F 23.34

Lowercase letters, a, b, and c, indicate pairwise mean

differences between sites (P £ 0.05; Tukey’s HSD test)

Ecological correlates of invasion by Arundo donax 595

123

influenced by year (P £ 0.0001), rhizome fresh

weight (P £ 0.0001), soil temperature (P £ 0.05),

soil moisture (P £ 0.0001), and percent bare ground

(P £ 0.01) (Table 3).

Site-specific correlates of A. donax performance

None of the independent variables in SD and OC

showed VIF ‡ 4.0, but percent bare ground and litter

depth in RIV had VIF ‡ 4.0 (Table 4). Litter depth was

removed from the analysis for RIV. Correlations

between independent variables were generally weak

(r \ 0.50), with the following exceptions: species

richness and diversity (r = 0.71); bare ground and litter

depth (r = –0.57); bare ground and species richness

(r = –0.52); bare ground and diversity (r = –0.55);

PAR and percent cover (r = –0.63) (data not shown).

When sites were considered singly over the years,

A. donax was more successful in certain sites and its

performance varied according to different variables at

each site. Shoot emergence time did not differ between

sites (Fig. 2A), but shoots survived longest in SD

(Fig. 2B) and attained the greatest height in RIV

(Fig. 2C). In SD, shoot emergence was inversely

related to PAR and herbivory (R2 = 0.26, Table 5). In

OC, none of the independent variables significantly

explained shoot emergence timing (data not shown). In

RIV, shoot emergence was inversely related to soil

temperature and moisture (R2 = 0.43, Table 5). In SD,

shoot survival was positively related to initial rhizome

fresh weight and herbivory, and inversely related toTa

ble

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0±

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erim

enta

lp

erio

dea

chy

ear

wer

en

ot

mo

nit

ore

d

Table 3 Analyses of covariance for A. donax shoot survival

and height with significant independent variables for all years

and all sites pooled (n = 200)

Response variable Independent variables F P

Shoot survival Site 11.45 0.0001

Model R2 = 0.49 Rhizome FW 13.72 0.0001

Soil moisture 10.05 0.002

Percent bare ground 5.22 0.023

Herbivory 18.58 0.0001

Shoot height Year 8.33 0.0001

Model R2 = 0.46 Rhizome FW 24.55 0.0001

Soil temperature 5.04 0.026

Soil moisture 41.10 0.0001

Percent bare ground 6.25 0.013

Community diversity, which was only measured in 2004 and

2005, was not included in the analysis. FW = fresh weight

596 L. D. Quinn, J. S. Holt

123

soil temperature (R2 = 0.50, Table 5). In OC, shoot

survival was positively linked with rhizome fresh

weight, soil moisture, and percent bare ground

(R2 = 0.57, Table 5). In RIV, shoot survival was

positively related to PAR, soil temperature and mois-

ture, and percent native cover (R2 = 0.71) (Table 5).

Shoot height was influenced by positive relationships

with rhizome fresh weight and herbivory and inverse

relationships with soil temperature and species

richness in SD (R2 = 0.56) (Table 5). For OC, height

was explained by positive relationships with rhizome

fresh weight, soil moisture, and percent bare ground

(R2 = 0.58) (Table 5). In RIV, shoot height was

positively related to PAR, soil temperature and mois-

ture, and percent native cover (R2 = 0.59) (Table 5).

Discussion

Evidence for a competitive-ruderal life history

for A. donax

Arundo donax is more likely to establish in field

conditions that provide bare ground and ample soil

moisture. These factors were positively related to

survival and height when considered across all sites

and years, and individually in at least two of the sites.

These conditions would be expected in the period

following seasonal flooding in a riparian area in

southern California’s Mediterranean climate. Such

seasonal floods remove litter and saturate soils that

then dry gradually throughout the drier months until

the next rainy season (Gasith and Resh 1999). Like the

disturbance-dependent natives that require flood-

scoured substrates and high levels of soil moisture

for germination (Stromberg 1997), A. donax seems to

take advantage of these wet conditions for rhizome

dispersal and rapid clone establishment. A. donax

rhizomes can sprout under a range of moisture

regimes from dry to wet, with cool temperatures

increasing success in wet conditions (Boose and Holt

1999). In the present study, soil temperature was

correlated with shoot height when all years and sites

were considered together, and with emergence in one

site. Like other ruderal species, growth rates in

A. donax are extremely rapid. A. donax has been

observed to grow 10 cm per day (Perdue 1958;

Dudley 2000). This may allow A. donax to preempt

and monopolize space and nutrients on newly exposed

floodbanks to the detriment of small-statured ruderals.

In contrast to most ruderal species, like Eschscholzia

californica (a California native) and Poa annua

(introduced), successfully established A. donax plants

quickly develop the perennial lignified shoots and

dense canopies (Bell 1997; Dudley 2000) typical of

plants with a competitive life history (Grime 1977).

While nitrogen and climate factors were measured

on too large a scale to be entered as plot variables,

these may have influenced the success of A. donax in

the three sites. Field and greenhouse studies have

shown that belowground lateral expansion in A.

donax increases in high-nitrogen soils compared with

low-nitrogen soils (Decruyenaere and Holt 2005;

Quinn et al. 2007). Pre-planting rhizome fresh weight

values were consistently greatest from the RIV site

(see Table 2), where nitrate levels were greatest. The

high productivity in this site may favor a more

competitive life history strategy in A. donax (Grime

1977), causing further displacement of the native

plant community.

Table 4 Variance inflation

factors (VIF) for each

independent variable in the

three sites. Because bare

ground and litter depth were

collinear (VIF [ 4) in RIV,

litter depth was removed

from multiple regression

analyses

Independent variables Variance inflation factor (VIF)

SD OC RIV RIV w/o litter depth

Rhizome FW 1.16 1.07 1.13 1.10

PAR 1.82 1.57 1.49 1.48

Soil temperature 1.28 2.03 2.89 2.65

Soil moisture 1.83 1.47 1.62 1.56

Bare ground 1.86 1.39 7.69 1.92

Litter depth 1.39 1.41 6.99

Native cover 1.69 2.09 2.92 2.87

Species richness 1.55 1.28 2.02 1.92

Herbivory 1.22 1.24 1.15 1.11

Ecological correlates of invasion by Arundo donax 597

123

Arundo donax rhizome size influences invasion

success

Vegetative reproduction is one of the traits conferring

advantage to invasive plants (Kolar and Lodge 2001;

Lloret et al. 2005), because the stored carbohydrates

in large rhizomes (Decruyenaere and Holt 2001) may

allow greater aboveground performance during early

establishment (Quinn 2006). For example, rhizome

size contributed positively to A. donax shoot height

and survival in an experiment that assessed the

invasibility of restored plots (Quinn 2006). In the

present study, rhizome fresh weight positively influ-

enced shoot height and survival overall and in two of

the three sites. Rhizome fresh weight did not

influence A. donax success in RIV, even though this

site had the largest rhizomes over all 3 years. This

may be due to the lack of variation in rhizome size

there, while the other sites had more variation within

and among years.

Arundo donax tolerates a wide range

of environmental conditions

Arundo donax has invaded riparian systems through-

out the United States, with populations in locations as

dissimilar as Maryland and southern California (Bell

1997). The ability of this species to sustain popula-

tions in such disparate regions suggests that it can

tolerate a wide variety of environmental conditions.

Even when examined on a finer scale, as in the

present study, A. donax displays the ability to

respond to small variations in the environment. While

certain common patterns were found, different vari-

ables predicted the success of this species in each of

the three southern California sites. Although efforts

were made to eliminate the effects of collinearity, it

can be difficult to interpret the combined effects of

field-measured variables. For example, shoot height

and survival time were influenced by temperature in

two sites, but the direction of the relationship differed

between the two locations. Single factor experiments

can illustrate physiological tolerance more clearly.

Neither root nor shoot production from A. donax

rhizome fragments were affected by temperatures

ranging from 5 to 35�C (Quinn 2006). Emergence

time and shoot height did not differ in shade

treatments ranging from approximately 18% of full

sun to 100% full sun (Quinn 2006). In another study,

A. donax was able to tolerate light levels as low as

10% of full sun (Spencer et al. 2005). It is likely,

therefore, that broad physiological tolerance contrib-

utes to the ability of this species to respond to

different environmental conditions. While phenotypic

0

10

20

30

40

50

60

70

80

90

Sh

oo

t em

erg

ence

(d

ays)

0

20

40

60

80

100

120

140

160

180

Sh

oo

t su

rviv

al (

day

s)

0

10

20

30

40

50

60

OC SD

Site

Sh

oo

t h

eig

ht

(cm

)

aaA

a

bB

aa

bC

aba

RIV

Fig. 2 Mean values (n = 200) for A. donax (A) shoot emer-

gence, (B) shoot survival, and (C) shoot height across three

southern California sites (Orange county [OC], Riverside

county [RIV], and San Diego county [SD]), pooled over three

years (2003–2005). Shoots that survived beyond the experi-

mental period each year were not monitored. Pairwise

differences (P £ 0.05; Tukey’s HSD) between sites are

indicated by lowercase letters

598 L. D. Quinn, J. S. Holt

123

plasticity was not tested in the present experiment per

se, plasticity in the face of environmental variation

has been identified as one of the attributes that

correlate with invasiveness across plant genera (Sakai

et al. 2001; Annapurna and Singh 2003; Sharma et al.

2005; Burns and Winn 2006; Richardson and Pysek

2006). A recent study states that the attributes that

confer the greatest potential for invasiveness change

throughout the course of an invasion, such that

species that are preadapted for disturbed habitats

succeed in the initial establishment phase, while

phenotypic plasticity seems to be more important in

the secondary spread phase (Dietz and Edwards

2006). With its dispersal by vegetative propagules,

broad physiological tolerance, and apparent ability to

dominate entire watersheds (Dudley 2000), A. donax

may fit this new model.

The role of biotic factors in establishment

of A. donax

While shoot height was negatively affected by species

richness in one site (SD), neither species richness nor

community diversity strongly influenced A. donax

performance overall. In a separate study that manip-

ulated native species richness, no relationship was

found between species richness and A. donax estab-

lishment (Quinn 2006). Instead, a particular native

species (Baccharis salicifolia) altered abiotic

Table 5 Results of

multiple regression analyses

for each site with all years

pooled

For the San Diego County

(SD) and Orange County

(OC) sites, n = 75, while

n = 50 for the Riverside

County (RIV) site due to its

inclusion in the experiment

for only two of the 3 years.

Only A. donax response

variables that were

significantly explained by

any combination of

independent variables are

shown. FW = fresh weight.

* P £ 0.05; ** P £ 0.01;

*** P £ 0.001

Response variable Independent variables Coefficient P

Oceanside, San Diego County

Shoot emergence PAR –0.74 0.05

Model R2 = 0.26 Herbivory –73.27 0.02*

Model P = 0.01

Shoot survival Rhizome FW 0.93 \0.0001***

Model R2 = 0.50 Soil temperature –13.59 0.001***

Model P = 0.0001 Herbivory 131.21 0.001***

Shoot height Rhizome FW 0.28 \0.0001***

Model R2 = 0.56 Soil temperature –3.67 \0.0001***

Model P = 0.0001 Species richness –6.58 0.02*

Herbivory 33.10 0.001***

Aliso Viejo, Orange County

Shoot survival Rhizome FW 0.29 0.01**

Model R2 = 0.57 Soil moisture 3.74 \0.0001***

Model P = 0.0001 Bare ground 0.97 \0.0001***

Shoot height Rhizome FW 0.21 \0.0001***

Model R2 = 0.58 Soil moisture 1.94 \0.0001***

Model P = 0.0001 Bare ground 0.34 0.01**

Riverside, Riverside County

Shoot emergence Soil temperature –23.28 \0.0001***

Model R2 = 0.43 Soil moisture –1.40 0.04*

Model P = 0.002

Shoot survival PAR 2.36 \0.0001***

Model R2 = 0.71 Soil temperature 15.28 \0.0001***

Model P = 0.0001 Soil moisture 1.43 \0.0001***

Native cover 1.07 0.04*

Shoot height PAR 0.88 0.01**

Model R2 = 0.59 Soil temperature 10.26 \0.0001***

Model P = 0.0001 Soil moisture 1.03 \0.0001***

Native cover 1.10 0.01**

Ecological correlates of invasion by Arundo donax 599

123

conditions in our experimental plots to the detriment

of A. donax (Quinn 2006). While we did not see a

strong effect of species richness or diversity in the

present study, it is likely that the native species in our

plots altered environmental conditions similarly. For

example, both diversity and species richness are

inversely related to bare ground, a factor that strongly

influenced A. donax performance.

Plant-herbivore interactions influenced perfor-

mance of A. donax across years and sites and in

one site. While it is counterintuitive that percent

herbivory was positively correlated with survival and

height, we suggest that these relationships are mere

artifacts of the data in that taller shoots with longer

lifetimes would be more likely to experience herbiv-

ory than shoots that remain small and senesce early.

Stimulation of growth seemed unlikely because,

while many chewed shoots did recover, they were

observed to be less vigorous than their unchewed

counterparts. However, mammalian herbivory of

A. donax has not been reported and we feel the

phenomenon is important enough to warrant future

investigations into herbivore identities and impacts

on new and existing A. donax plants.

Management recommendations

As demonstrated here and in other studies, the

exploitation of the vegetative reproduction strategy

by A. donax nearly guarantees that rhizomes will

sprout regardless of initial size or environmental

conditions (Decruyenaere and Holt 2001; Quinn

2006). Therefore, when removing large clones of

A. donax in any riparian area, it is essential to

completely kill or remove all living rhizome pieces

and to work downstream from the top of a watershed

to prevent reinvasion of removal areas. This study

revealed that long-term survival and development

into large spreading clones, however, seems to

depend on site factors. Because conditions that are

most favorable for A. donax survival, including bare

soil and high soil moisture levels are most likely to be

found near the water’s edge, it may be most effective

for managers to prevent future spread by targeting

large rhizomes sprouting on floodbanks. Following

removal of upstream clones and new sprouts, stabil-

ization of streambanks by revegetation with diverse

mixtures of natives may also decrease the likelihood

of A. donax survival.

Acknowledgements We wish to thank the anonymous

reviewers for insightful comments on the first draft of this

manuscript. We appreciate the field assistance of Sarah Otter,

Kenny Ahlrich, Mike Rauterkus, and Virginia White. We

would also like to thank the California Department of Food and

Agriculture and the Riverside County Endowment to the

Shipley-Skinner UC Reserve for grant funding.

References

Annapurna C, Singh JS (2003) Phenotypic plasticity and plant

invasiveness: case study of congress grass. Curr Sci

85:197–201

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

5:1–24

Beerling DJ (1993) The impact of temperature on the northern

distribution limits of the introduced species Fallopiajaponica and Impatiens glandulifera in north-west

Europe. J Biogeogr 20:45–53

Bell GP (1997) Ecology and management of Arundo donax,

and approaches to riparian habitat restoration in southern

California. In: Brock J, Wade M, Pysek P, Green D (eds)

Plant invasions: studies from North America and Europe.

Backhuys, Leiden, Netherlands, pp 103–113

Blumenthal DM (2006) Interactions between resource avail-

ability and enemy release in plant invasion. Ecol Lett

9:887–895

Boose AB, Holt JS (1999) Environmental effects on asexual

reproduction in Arundo donax. Weed Res 39:117–127

Bowman RH (1973) Soil survey, San Diego area, California.

Department of Agriculture, Soil Conservation Service,

Washington, DC

Burke MJW, Grime JP (1996) An experimental study of plant

community invasibility. Ecology 77:776–790

Burns JH, Winn AA (2006) A comparison of plastic responses

to competition by invasive and non-invasive congeners in

the Commelinaceae. Biol Invasions 8:797–807

Caplan JS, Yeakley JA (2006) Rubus armeniacus (Himalayan

blackberry) occurrence and growth in relation to soil and

light conditions in western oregon. Northwest Sci 80:9–17

Chatterjee S, Hadi AS, Price B (2000) Regression analysis by

example. John Wiley and Sons, New York, NY

Crawley MJ (2003) The structure of plant communities. In:

Crawley MJ (ed) Plant ecology. Blackwell Publishing,

Malden, MA, pp 475–531

Decruyenaere JG, Holt JS (2001) Seasonality of clonal prop-

agation in giant reed. Weed Sci 49:760–767

Decruyenaere JG, Holt JS (2005) Ramet demography of a

clonal invader, Arundo donax (Poaceae), in southern

California. Plant Soil 277:41–52

Dietz H, Edwards PJ (2006) Recognition that causal processes

change during plant invasion helps explain conflicts in

evidence. Ecology 87:1359–1367

Dodd MB, Barker DJ, Wedderburn ME (2004) Plant diversity

effects on herbage production and compositional changes

in New Zealand hill country pastures. Grass Forage Sci

59:29–40

Dudley T (2000) Arundo donax. In: Bossard CC, Randall JM,

Hoshovsky MC (eds) Invasive plants of California’s

600 L. D. Quinn, J. S. Holt

123

wildlands. University of California Press, Berkeley, CA,

pp 53–58

Elton CS (1958) The ecology of invasions by animals and

plants. Methuen, London, England, 181 pp

Fenn ME, Baron JS, Allen EB, Rueth HM, Nydick KR, Geiser

L, Bowman WD, Sickman JO, Meixner T, Johnson DW,

Neitlich P (2003) Ecological effects of nitrogen deposition

in the western United States. Bioscience 53:404–420

Fox J (1997) Applied regression analysis, linear models, and

related methods. Sage Publications, Thousand Oaks, CA

Gasith A, Resh VH (1999) Streams in Mediterranean climate

regions: abiotic influences and biotic responses to pre-

dictable seasonal events. Annu Rev Ecol Syst 30:51–81

Graham MH (2003) Confronting multicollinearity in ecological

multiple regression. Ecology 84:2809–2815

Grime JP (1977) Evidence for existence of 3 primary strategies

in plants and its relevance to ecological and evolutionary

theory. Am Nat 111:1169–1194

Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC,

Harris CJ, Licari D (2005) Life-history correlates of plant

invasiveness at regional and continental scales. Ecol Lett

8:1066–1074

Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and

invasion: implications for conservation. Conserv Biol

6:324–337

Huston MA (2004) Management strategies for plant invasions:

manipulating productivity, disturbance, and competition.

Divers Distrib 10:167–178

Kennedy TA, Naeem S, Howe KM, Knops JMH, Tilman D,

Reich P (2002) Biodiversity as a barrier to ecological

invasion. Nature 417:636–638

Khudamrongsawat J, Tayyar R, Holt JS (2004) Genetic

diversity of giant reed (Arundo donax) in the Santa Ana

River, California. Weed Sci 52:395–405

Kolar CS, Lodge DM (2001) Progress in invasion biology:

predicting invaders. Trends Ecol Evol 16:199–204

Levine JM (2000) Species diversity and biological invasions:

relating local process to community pattern. Science

288:852–854

Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of

biotic resistance to exotic plant invasions. Ecol Lett

7:975–989

Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K,

Lavorel S (2003) Mechanisms underlying the impacts of

exotic plant invasions. Proc R Soc Lond B Biol Sci

270:775–781

Lloret F, Medail F, Brundu G, Camarda I, Moragues E, Rita J,

Lambdon P, Hulme PE (2005) Species attributes and

invasion success by alien plants on Mediterranean islands.

J Ecol 93:512–520

Mack RN (1996) Predicting the identity and fate of plant

invaders: Emergent and emerging approaches. Biol Con-

serv 78:107–121

Meekins JF, McCarthy BC (2001) Effect of environmental

variation on the invasive success of a nonindigenous

forest herb. Ecol Appl 11:1336–1348

Myers CV, Anderson RC, Byers DL (2005) Influence of

shading on the growth and leaf photosynthesis of the

invasive non-indigenous plant garlic mustard [Alliariapetiolata (M. Bieb) Cavara and Grande] grown under

simulated late-winter to mid-spring conditions. J Torrey

Bot Soc 132:1–10

Myers RH (1986) Classical and modern regression with

applications. Duxbury Press, Boston, MA

Naeem S, Knops JMH, Tilman D, Howe KM, Kennedy T,

Gale S (2000) Plant diversity increases resistance to

invasion in the absence of covarying extrinsic factors.

Oikos 91:97–108

OCWD (2004) Orange County water district natural resources

news. Fountain Valley, CA, p 2

Perdue RE (1958) Arundo donax: source of musical reeds and

industrial cellulose. Econ Bot 12:368–404

Prieur-Richard AH, Lavorel S, Dos Santos A, Grigulis K

(2002) Mechanisms of resistance of Mediterranean annual

communities to invasion by Conyza bonariensis: effects

of native functional composition. Oikos 99:338–346

Quinn LD (2006) Ecological correlates of invasion by Arundodonax. Dissertation, Ph.D. Dissertation. Botany and Plant

Sciences, University of California, Riverside, Riverside,

California

Quinn LD, Rauterkus MA, Holt JS (2007) Effects of nitrogen

enrichment and competition on growth and spread of giant

reed (Arundo donax). Weed Sci 55:319–326

Rejmanek M, Richardson DM (1996) What attributes make

some plant species more invasive? Ecology 77:1655–1661

Richardson DM, Pysek P (2006) Plant invasions: merging the

concepts of species invasiveness and community invasi-

bility. Prog Phys Geogr 30:409–431

Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J,

With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand

NC, McCauley DE, O’Neil P, Parker IM, Thompson JN,

Weller SG (2001) The population biology of invasive

species. Annu Rev Ecol Syst 32:305–332

Sharma GP, Singh JS, Raghubanshi AS (2005) Plant invasions:

emerging trends and future implications. Curr Sci 88:726–

734

Spencer DF, Ksander GG, Liow PS (2005) Response of giant

reed (Arundo donax L.) to intermittent shading. In: Ne-

therland MD (ed) 45th Annual meeting of the Aquatic

Plant Management Society, Inc., Aquatic Plant Manage-

ment Society, Inc., San Antonio, TX

Stohlgren TJ, Binkley D, Chong GW, Kalkhan MA, Schell LD,

Bull KA, Otsuki Y, Newman G, Bashkin M, Son Y (1999)

Exotic plant species invade hot spots of native plant

diversity. Ecol Monogr 69:25–46

Stromberg JC (1997) Growth and survivorship of Fremont

cottonwood, Goodding willow, and salt cedar seedlings

after large floods in central Arizona. Great Basin Natu-

ralist 57:198–208

Wachtell JK (1978) Soil survey of Orange County, and western

part of Riverside County, California. Department of

Agriculture, Soil Conservation Service, Washington, DC

Ecological correlates of invasion by Arundo donax 601

123