Do Higher Resource Capture Ability and Utilization Efficiency Facilitate the Successful Invasion of Exotic Plant? A Case Study of <i>Alternanthera philoxeroides</i>

doi:10.4236/ajps.2013.49226

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American Journal of Plant Sciences, 2013, 4, 1839-1845

http://dx.doi.org/10.4236/ajps.2013.49226 Published Online September 2013 (http://www.scirp.org/journal/ajps)

Do Higher Resource Capture Ability and Utilization

Efficiency Facilitate the Successful Invasion of Exotic Plant?

A Case Study of Alternanthera philoxeroides

Xuyan Geng, Shang Jiang, Bo Li, Xiaoyun Pan*

Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science &

Ecological Engineering, Institute of Biodiversity Science, Shanghai, China.

Email: *[email protected]

Received June 16th, 2013; revised July 20th, 2013; August 20th, 2013

which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

We tested the hypothesis that introduced populations may have higher resource capture ability and utilization efficiency

than native ones of invasive plants. We compared ecophysiological traits including maximum photosynthetic rate (Pmax),

apparent quantum yield (Q), specific leaf area (SLA), photosynthetic energy use efficiency (PEUE), photosynthetic ni-

trogen use efficiency (PNUE), water use efficiency (WUE), mass-based and area-based leaf construction cost (CCmass

and CCarea), and mass-based and area-based leaf nitrogen concentration (Nmass and Narea) between native (Argentina) and

introduced (USA) populations of two varieties (North Apa and South Apo) of Alternanthera philoxeroides under com-

mon garden conditions in China. For Apo and Apa, Pmax, Q, Nmass and WUE were not significantly different between

native and introduced populations; introduced populations had significantly lower SLA and lower CCmas s but signifi-

cantly higher Narea and CCarea than native ones. For Apa, the introduced populations showed significantly lower PEUE

and lower PNUE while for Apo, PEUE and PNUE were not significantly different between native and introduced

populations. The results indicated that introduced populations of A. philoxeroides do not show higher resource capture

ability and resource utilization efficiency than their native ones in the common garden experiment, suggesting that these

traits may not necessarily contribute to successful invasion of invasive plants.

Keywords: Invasive Plant; Resource Use Efficiency; Construction Cost; Leaf Nitrogen

1. Introduction

One mechanism which has been frequently mentioned

and investigated empirically in the context of plant inva-

sions is that higher resource capture ability and utiliza-

tion efficiency may facilitate successful invasion [1-3].

Studies comparing leaf traits of invasive plants and na-

tive plants have shown that invasive species have higher

specific leaf area (SLA) [4,5], lower mass-based leaf

construction cost (CCma s s ) [4,6-8], higher photosynthetic

nitrogen use efficiency (PNUE) [3,4,9], higher photo-

synthetic energy use efficiency (PEUE) [8,10] and higher

water use efficiency (WUE) [9,11] than native species.

However, some studies have detected that there are no

significant differences in CCmass [12], PNUE [8] and

WUE [6,8] between invaders and natives. A recent study

also suggests that the populations in the introduced range

of an invasive species have evolved a higher PEUE and a

shorter payback time but not lower CCmass than those in

the native range [13].

Do exotic invasive plants have generally evolved higher

resource capture ability and utilization efficiency in their

introduced ranges? To answer this question, we com-

pared leaf-level physiological traits that are related to re-

source capture and utilization efficiency, e.g., maximum

photosynthetic rate (Pmax), apparent quantum yield, SLA,

PNUE, PEUE, WUE, area-based leaf construction cost

(CCarea) and CCmass, area-based leaf nitrogen contention

(Narea) and mass-based nitrogen contention (Nmass), be-

tween native (Argentina) and introduced (USA) popula-

tions of two varieties of Alternanthera philoxeroides (al-

ligator weed) under common garden conditions in Shang-

hai, China.

*Corresponding author.

Do Higher Resource Capture Ability and Utilization Efficiency Facilitate the Successful Invasion

of Exotic Plant? A Case Study of Alternanthera philoxeroides

1840

2. Materials and Methods

2.1. Plant Species

Alternanthera philoxeroides (alligator weed), a clonal

herbaceous perennial native to South America, is distrib-

uted from Buenos Aires province to southern Brazil

(18˚S - 39˚S) [14]. It has been widely introduced to warm

temperate and subtropical humid areas in North America,

Australia and China [15]. At present, A. philoxeroides is

one of the most noxious weeds in wetlands and agro eco-

systems [16]. Many attributes have contributed to the in-

vasion success of A. philoxeroides in China, such as ra-

pid vegetative growth and reproduction [15], higher phe-

notypic plasticity than its native congener A. sessilis [16,

17] and adaptation to physical disturbances[18].

A. philoxeroides typically emerges from belowground

buds (on storage roots) in spring and then spreads vege-

tatively throughout a growing season, consequently form-

ing dense monospecific stands. It overwinters with stor-

age roots and rhizomes [18]. Although A. philoxeroides

may produce viable seeds, sexual reproduction contrib-

utes little to population regeneration due to extremely

low seed outputs and low germination rates [14,15]. In

contrast, vegetative propagation (with storage roots and

stems) is its primary regeneration strategy in the field

[14].

At least two varieties of A. philoxeroides are recog-

nized in Argentina [19]: the northern A. p. var. acutifo lia

(Apa) and the southern A. p. var. obtusifolia (Apo) [20].

The two varieties are distributed in different geographic

areas and habitat types (Figure 1(a); Flooding Pampa

grasslands vs. wetlands along the Middle Parana River),

and have evolved different leaf and stem morphologies

[19,20]. Both Apa and Apo have been introduced into

USA (Figure 1(b)) [21].

In 2003 and 2004 we sampled stem fragments of A.

philoxeroides from 16 populations: eight Argentina po-

pulations and eight USA populations (Figure 1). Both

Argentina and USA populations were sampled widely

across their distribution range. We collected 10 - 20 stems

for each population (more than 20 m apart from each

other to ensure that different clones/genets might be sam-

pled). All collected stems were cloned in a greenhouse

for more than 3 years to reduce environmental maternal

effects.

2.2. Experiment Design

The study was carried in August 2012 at the Experimen-

tal Field Unit of Fudan University, Shanghai, China,

which is an outdoor field previously used for other gar-

den experiments. The climate is humid subtropical, with

rainfall averaging 1160 mm per year and with mean

monthly temperatures ranging from 27.9˚C in July to

(a) Argentina

CH FO

(b) USA

TA LA

GULF OF MEXICO

Figure 1. Sample sites of two varieties, Apa (black circle)

and Apo (black triangle), of Alternanthera philoxeroides

from native (Argentina) and introduced (USA) range.

4.2˚C in January. In July 2011, we vegetative cloned 16

populations in experiment garden. Two weeks later we

selected four individuals (with 2 - 3 internodes and four

or six leaves) per populations, and planted them individu-

ally at a depth of 2 cm in round pots (diameter, 23 cm;

depth, 18 cm).We used nutrient soil (Beilei, Beilei Organic

Fertilizer Co., Ltd., Zhenjiang, China) with the content of

N, P, K ≥ 2% (dry weight basis), organic matter ≥ 35%

(dry weight basis), water ≤ 45%, and pH 5.5 - 6.5. All

pots were randomly arranged on a desk and re-random-

ized weekly to reduce position effects. Pots were watered

by hand every other day to keep the substrate moist.

We harvested all plant materials 8 weeks after planting.

Each plant was separated into leaves, stems, and roots.

We determined leaf area for each plant with a leaf area

meter (LI-3100A; LI-COR, Lincoln, NB, USA). All ma-

terials were oven dried at 55˚C for 72 h and then weighed

to the nearest 0.001 g. SLA (cm2·g–1) was calculated as

the ratio of leaf area to leaf dry mass. And then we finely

ground the dried leaves.

Mass-based carbon concentration (C) and Nmass of the

powdered leaves were determined with OEA analyzer

(Organic Elemental Analysis, FlashEA1112, Thermo Fin-

nigan, Italy). Ash concentration (Ash) was determined

after combusting leaf sample in a muffle furnace at

550˚C for 6 h. Ash alkalinity (AA) was determined aci-

dimetrically [22]. The mineral concentration (Min) of

Do Higher Resource Capture Ability and Utilization Efficiency Facilitate the Successful Invasion

of Exotic Plant? A Case Study of Alternanthera philoxeroides

1841

each sample was calculated according to [22] as follows:

MinAsh AA30 Nitrate, (1)

CCmass can be calculated [23,24] as follows:

CC1.041 5.077 1000 Min

1000 MinNorg

5.325 .

1000 1000



 



















(2)

Narea and Nmass), with range (Argentina vs. USA) as a

fixed factor, population nested within range as a random

factor. The residuals for all tests were normally distrib-

uted and no transformations were necessary. All analyses

were carried out using SPSS 13.0 (SPSS, Chicago, USA).

3. Results

For both Apo and Apa, Pma x (Figure 2(a)) and apparent

quantum yield (Figure 2(b)) were not significantly dif-

ferent between native and introduced populations, and

introduced populations had significantly lower SLA

(Figure 2(c)).

Nitrate concentration were negligible, thus we as-

sumed that Norg = Nmass [25].

2.3. Determination of Physiological Traits For Apa the introduced populations showed signifi-

cantly lower PEUE and PNUE, while for Apo, PEUE and

PNUE were not significantly different between native

and introduced populations (Figures 3(a) and (b)). For

both Apa and Apo, WUE were not significantly different

between native and introduced populations (Fi gure 3(c )).

Net photosynthetic rate in relation to varying photosyn-

thetic photon flux density (light response curves) was

determined on the youngest fully-expanded leaves with a

Li-6400 Portable Photosynthesis System (LI-6400; LI-

COR, Lincoln, NB, USA). Measurements were made on

2 - 3 representative leaves on 4 individuals of each varie-

ties in a pair during continuously sunny days from 09:00

to 12:00 am in the field in August 2012. All leaves of the

Argentina and USA populations in a pair were of similar

age and position on the stems. PPFD decreased in a step-

wise fashion from 2000 to 0 µmol photon m–2·s–1 (at

2000, 1500, 1200, 1000, 800, 600, 400, 200, 150, 100, 70,

50, and 0). During the measurements, CO2 concentration,

temperature and relative humidity within the leaf cham-

ber were similar to those of ambient conditions. Each

leaf was acclimated for 10 - 20 min to 2000 µmol photon

m–2·s–1 of PPFD prior to the measurement.

For both Apa and Apo, Nmas s were not significantly

different between native and introduced populations (Fig-

ure 4(a)), but introduced populations had significantly

higher Narea than native ones (Figure 4). Introduced po-

pulations showed significantly lower CCmass (Figure

4(c)), but significantly higher CCarea (Figure 4(d)) than

native ones.

4. Discussion

4.1. Resource Capture Ability

Our results showed that introduced populations of A. phi-

loxeroides showed no significant difference in Pmax, ap-

parent quantum yield, and Nmass relative to the native po-

pulations, suggesting that invasive populations of A. phi-

loxeroides do not have advantage in resource capture

ability compared to their native populations. This result

was inconsistent with previous studies. Previous studies

have found that most invasive plants have higher Pmax

[6,9,11] compared to their co-occurring natives. Ref [8]

found that invasive species had significantly higher Pmax

(mass-based) than their non-invasive alien congeners. In

a study of comparing the functional traits between plants

from invasive and native populations of alien plant,

higher Pmax and higher SLA of invasive populations was

also found [13].

We fitted entire light response curves using the non-

rectangular hyperbola model according to [26] as shown

in Equation (3), where Photo is the leaf net photosynthe-

sis rate, PAR is the light intensity, Pmax is maximum

photosynthetic rate, Q is apparent quantum yield, R is

dark respiration rate and K is a constant.

Narea (g·m–2) = Nmass/SLA;

CCarea (g·glucose·m–2) = CCmass/SLA;

PEUE (µ·mol CO2 g glucose–1·s–1) = Pmax/CCarea [6];

PNUE (µ·mol CO2 g–1·s–1) = Pmax/Narea [27];

WUE (µ·molCO2 µmol–1 H2O) = Pmax/E (transpiration)

[9,28].

2.4. Statistical Analysis SLA can be envisaged as an indicator of thickness or

density; leaves with a higher SLA are typically thin and

have greater levels of herbivory [29]. Our results showed

that invasive plants of A. philoxeroides had significantly

lower SLA than their corresponding natives, indicating

Nested analysis of variance (ANOVA) was used to com-

pare if there had differences between plants from inva-

sive and native populations in parameters (Pmax, apparent

quantum yield, SLA, PNUE, PEUE,WUE, CCarea, CCmass,



max maxmax

PAR QPPAR QP4PAR QPK

Photo R.

 



 (3)

Do Higher Resource Capture Ability and Utilization Efficiency Facilitate the Successful Invasion

of Exotic Plant? A Case Study of Alternanthera philoxeroides

1842

(a)

ative Introduced

Apo Apa

NS NS

(b)

Apo Apa

(c)

Apo Apa

100

150

200

250

300

Specific leaf area (SLA)

(cm

·g

-1

)

0.00

0.02

0.04

0.06

Maximum photosynthetic rate

(μmol CO

-2

·s

-1

)

Apparent quantum yield

(μmol CO

per μmol photone)

Figure 2. Differences in maximum photosynthetic rate (Pmax

(a), apparent quantum yield (b) and speci fic leaf area (SLA)

pulations of two varieties (Apo and Apa) of Alternanthera

philoxeroides. Dates are means ± SE (NS, no significant dif-

ferences, *P < 0.05).

introduced populations of A. philoxeroides may have

evolved higher resistance to generalist herbivores than

native ones (Pan et al. unpublished results).

4.2. Resource Utilization Efficiency

Our results showed that invasive Apa had significantly

lower PEUE and PNUE than native Apa, and invasive

(a)

ative Introduced

Apo Apa

PEUE

(μmol CO2 g·glucose-1·s-1)

0.4

0.3

0.2

0.1

0.0

(b)

Apo Apa

PNUE

(μmol CO2 g-1·s-1)

(c)

Apo Apa

WUE

(μmol CO2 μmol-1 H2O)

Figure 3. Differences in photosynthetic energy use efficiency

(PEUE) (a), photosynthetic nitrogen use efficiency (PNUE)

(b) and water use efficiency (WUE) (c) between native (Ar-

gentina) and introduced (USA) populations of two varieties

(Apo and Apa) of Alternanthera philoxeroides. Dates are

means ± SE (NS, no significant differences, *P < 0.05 and

**P < 0.01).

Apo had no significant difference in PEUE and PNUE

compared to native Apo. These results indicate that in-

troduced populations of A. philoxeroides do not have

higher resource utilization efficiency than their native

ones in the common garden experiment. This contrasts

Do Higher Resource Capture Ability and Utilization Efficiency Facilitate the Successful Invasion

of Exotic Plant? A Case Study of Alternanthera philoxeroides

1843

(b)

ative Introduced

Apo Apa

area

(g·m

-3

)

mass

(%)

0.0

0.5

1.0

1.5

2.0

(c)

(d)

Apo Apa

0.0

0.5

1.0

1.5

area

(g·glucose·m

-2

)

mass

(g·glucose·m

-1

)

Figure 4. Differences in mass-based nitrogen concentration

(Nmass) (a) area-based nitrogen concentration (Narea) (b)

mass-based construction cost (CCma ss ) (c) and area-based

construction cost (CCarea) (d) between native (Argentina)

and introduced (USA) populations of two varieties (Apo

and Apa) of Alternanthera philoxeroides. Dates are means ±

SE (NS, no significant differences, * P < 0.05, ** P < 0.01 and

***P < 0.001).

with previous studies. Invasive plants have often higher

PNUE [4,9,30], higher PEUE [8] or both higher PEUE

and PNUE [6,10,12] than natives species. Also in their

work comparing energy use strategy of an invasive spe-

cies from populations of its native ranges and introduced

ranges, Ref. [13] found that plants from invasive popula-

tions had a higher PEUE than native populations.

Our results showed that invasive populations of A. phi-

loxeroides had significantly lower CCmass and the same

levels of Nmass compared with native populations. How-

ever, due largely to significantly lower SLA, invasive

populations had significantly higher CCarea and Narea than

native populations (Figure 4). Nitrogen allocation to the

photosynthetic apparatus is suggested to be a major fac-

tor responsible for the interspecific variation in PNUE

[31]. Introduced Apa had the same leaf Nmass but signifi-

cantly lower PNUE than native ones, suggesting a de-

creased fraction of leaf nitrogen invested in the photo-

synthetic apparatus in introduced plants of Apa.

WUE did not differ between native and invasive po-

pulations of A. philoxeroides, which is accordant with

previous results that invasive plants are not at an advan-

tage over native species in WUE [6,8,9].

Our finding that introduced populations of A. philox-

eroides do not have higher resource capture ability and

resource utilization efficiency than their native ones in

the common garden experiment, suggesting that these

traits may not necessarily contribute to successful inva-

sion of invasive plants.

The importance of resource use efficiency will vary

across habitats and timescales [6]. Future research will be

needed to examine if there are differences in resource

capture ability and utilization efficiency between intro-

duced and native populations of invasive plants across

resource gradients and across their whole growth sea-

sons.

5. Acknowledgements

This study was financially supported by the National Na-

tural Science Foundation of China (31070369).

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