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J Plant Res (2009) 122:6979

DOI 10.1007/s10265-008-0197-1

REGULAR PAPER

Structural and physiological responses of two invasive weeds,


Mikania micrantha and Chromolaena odorata, to contrasting
light and soil water conditions
Ling-Ling Zhang Da-Zhi Wen

Received: 20 February 2008 / Accepted: 8 October 2008 / Published online: 22 November 2008
The Botanical Society of Japan and Springer 2008

Abstract To better understand the requirement of light


and soil water conditions in the invasion sites of two
invasive weeds, Mikania micrantha and Chromolaena odorata, we investigated their structural and physiological
traits in response to nine combined treatments of light [full,
medium and low irradiance (LI)] and soil water (full,
medium and low field water content) conditions in three
glasshouses. Under the same light conditions, most variables for both species did not vary significantly among
different water treatments. Irrespective of water treatment,
both species showed significant decreases in maximum
light saturated photosynthetic rate (Pmax), photosynthetic
nitrogen-use efficiency, and relative growth rate under LI
relative to full irradiance; specific leaf area, however,
increased significantly from full to LI though leaf area
decreased significantly, indicating that limited light availability under extreme shade was the critical factor
restricting the growth of both species. Our results also
indicated that M. micrantha performed best under a high
light and full soil water combination, while C. odorata was
more efficient in growth under a high light and medium soil
water combination.
Keywords Leaf morphology  Nmass content 
Photosynthesis  Photosynthetic nitrogen-use efficiency

L.-L. Zhang  D.-Z. Wen (&)


Institute of Ecology, South China Botanical Garden,
Chinese Academy of Sciences,
510650 Guangzhou, China
e-mail: dzwen@scib.ac.cn

Introduction
Alien plant invasion is a serious threat to natural and seminatural ecosystems worldwide (Mgidia et al. 2007), and
invasive plants that could successfully colonize a broad
range of habitats usually need structural and physiological
acclimation to variable environments and resources (Baker
1974).
Mikania micrantha Kunth and Chromolaena odorata L.
are two of the most notorious invasive weeds in southern
China. Both weeds originate from the Asteraceae family,
with M. micrantha being a perennial herbaceous weed vine
native to tropical Central and South America (Holm et al.
1977a; Cock 1982), whereas C. odorata is a perennial
herbaceous shrub native to Mexico, the West Indies and
tropical South America (Holm et al. 1977b). In its original
region, M. micrantha was abundant in open habitats and
showed poor growth performance under 25% shade (Ipor
1991); C. odorata grew on a wide range of soils and
favored 6070% relative soil water content, but performed
poorly when the relative soil water content exceeded 80%
(Vanderwoude et al. 2005). Although the distribution sites
of the two weeds differ in southern China, they sometimes
occur in the same habitat, such as in Guangzhou. Due to
their high competitiveness, and ability to spread and
establish rapidly, both species have invaded a wide range
of areas in southern China since the late 1980s (Xie et al.
2000; Li et al. 2006), and have caused serious damage to
semi-natural forests, pastures, crops and plantations (Zan
et al. 2000; Feng et al. 2002).
Light, water and nutrients are the main resources regulating the survival, growth and distribution of plants. Most
previous studies on these two species in response to
varying environments each focused on a single factor,
either light or drought (Wen et al. 2000; Wang et al. 2003).

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Several studies showed that both M. micrantha and C.


odorata were light-favoring species, with soil fertilizer
being less important for their invasion (Wen et al. 2000;
Huang et al. 2000; Wang et al. 2003; Vanderwoude et al.
2005). Others demonstrated that drought significantly
decreased growth of M. micrantha seedlings (Yang et al.
2005). However, a knowledge of how these two invasive
weeds respond to light and soil water interactions with
respect to their structural and physiological traits is
important in understanding their ecophysiological acclimation, which is not yet adequately understood.
Leaf structural and functional traits affect plant physiological performance. Specific leaf area (SLA) has proved a
good indicator of many important physiological characteristics, including leaf nutrient concentration, photosynthetic
capacity, plant relative growth rate (RGR) and its contributing components (Reich et al. 1999). These parameters,
along with leaf area ratio (LAR), water use efficiency
(WUE) and photosynthetic nitrogen use efficiency (PNUE),
are commonly employed to analyze and compare adaptation
mechanisms of plants naturally occurring in rich or poor
habitats, and to explain why and how some plants outperform others (Poorter 1989). On the other hand, phenotypic
plasticity has been hypothesized as one of the decisive plant
traits allowing a species to become invasive in newly colonized habitats (Dukes and Mooney 1999). The phenotypic
plasticity index [(maximum value-minimum value)/maximum value] is a simple parameter that can be used to assess
the extent of plant responsiveness to the environment for
variables with different units and ranges of variation (Valladares et al. 2000), and has been successfully employed to
describe the response of variables to contrasting light and
soil water conditions (Quero et al. 2006).
This study was carried out in three field glasshouses
with established seedlings of the two weeds grown under
three levels of light and three levels of soil moisture conditions with the objectives of: (1) determining the changes
in structural and physiological traits of the two invasive
weeds in response to different light and soil water conditions; (2) assessing how regional or local variations in light
and soil water may affect the growth advantages and
potential expansion of the two weeds, within a given climate; and (3) characterizing the functional relationships
among the variables.

treatment, has six separate plots for soil water treatment of


each species (1.5 m length 9 1.2 m width 9 0.5 m
height). Soils of 35 cm in depth for each plot were collected
from the surface layer (020 cm) of a forested site near the
garden, and transported to the experimental site and mixed
uniformly, and were adequate for both species to complete
their development during the first growing season.

Materials and methods

Site description

where qb and qw are bulk and water density (g cm-3), and


w is the gravimetric water content (%) (He et al. 2004).
At 4-day intervals, light intensity was measured at noon
using a photometer (LI-185B, Li-Cor, Lincoln, NE), and
soil water content was measured at 1700 hours by time

The experiment was carried out in three glasshouses located


in the South China Botanical Garden, Guangzhou (23080 N,
113170 E). Each glasshouse, representing one light

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Plant materials and multiplication


Seeds of M. micrantha were collected from Shenzhen city
(22270 22520 N, 113460 114370 E), Guangdong province, and those of C. odorata from Changjiang city
(18530 19300 N, 108380 109170 E), Hainan province, in
early spring of 2006. Fully developed and average-sized
seeds for each species were selected and sown separately in
20 pots (2.5 L volume) on 23 April 23 2006; after 4 weeks,
the seedlings developed were transferred to a 1.5 m 9
1.5 m plot for uniform growth under partial shade. In
early July 2006, 30 seedlings of about 90 cm height for M.
micrantha and 25 cm height for C. odorata were transferred to each plot and grown under optimal light and soil
water conditions for growth stability.
Light and water treatments
On 24 July 2006, seedlings of about 90 days old were
subjected to combined light and water treatments. Light
levels were set separately in three glasshouses as: (1) full
irradiance treatment (FI), receiving available radiation
inside the glasshouse; (2) medium-irradiance treatment
(MI), covered by a black nylon shade netting (2535% of
available radiation); and (3) low irradiance treatment (LI),
covered by one black and one gray nylon shade netting
(35% of available radiation) (Table 1). The soil water
treatments were: (1) full water (FW), well watered and kept
at 7090% of field water capacity; (2) medium water (MW),
kept at 3555% of field water capacity; (3) low water (LW),
with no additional watering and soil water content at
6.712.7% of field water capacity at that time (Table 1).
Water content at field capacity of soils outside the
glasshouses was 25.5%, on average, gravimetric and bulk
density was 1.16 g cm-3, as tested according to Li et al.
(2000). The volumetric water content (h) was calculated
using the equation:
qb
w
qw

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71

Table 1 Soil water content measured with time domain reflectometry


(TDR) and light irradiance at the beginning, middle and end of the
experiment (mean SE); and air temperature, air relative humidity
Time (days) FI
FW

and soil temperature during the experiment (mean SE) in three


glasshouses under the light and water conditions shown

MI
MW

LW

FW

LI
MW

LW

FW

MW

LW

Soil water content (%)


Mikania micrantha
0

23.6 1.27

13.7 0.40

6.7 0.97 22.9 1.04

15.9 0.89 10.1 1.01 23.8 1.42 15.2 0.74 11.8 1.28

36

21.2 1.18

12.6 0.77

4.5 0.67 21.8 1.85

10.5 0.56

72

24.4 0.97

16.7 0.45

4.0 0.59 25.6 1.99 17.34 0.55

6.2 0.80 24.9 1.64 14.2 1.41 10.1 1.41


6.3 0.88 27.4 1.25 15.0 1.07

7.9 0.67

Chromolaena odorata
0

21.9 1.52

14.0 1.45

8.4 0.99 23.3 1.15

13.5 0.30 10.6 0.35 26.0 0.83 15.7 1.32 12.7 1.29

36

24.3 1.37

14.1 0.66

4.7 0.15 24.1 0.70

11.2 1.20

6.3 0.70 24.5 1.11 14.2 1.16 10.6 0.44

72

27.1 1.15

18.9 1.87

3.7 0.70 28.1 1.38

18.4 0.40

5.4 1.19 28.8 1.04 15.0 1.26

7.3 0.88

Light irradiance (lmol photons m-2 s-1)


M. micrantha
0a

498.0 4.90

128.0 2.55

17.2 0.97

36

808.0 16.55

276.0 7.48

19.0 1.18

72

756.0 2.45

256.0 2.45

27.0 1.22

C. odorata
0

490.0 5.16

121.3 1.12

17.8 0.92

36

800.0 12.65

255.0 4.47

20.5 0.45

72

757.5 2.24

257.5 2.24

27.5 1.29

Air temperature, air relative humidity and soil temperature


Air temperature (C)

31.5 0.58

31.4 0.57

31.3 0.54

Air relative humidity (%)

65.9 3.46

70.3 3.10

64.3 3.53

Soil temperature (C)

29.8 0.41

29.5 0.39

29.0 0.38

FI Full irradiance, MI medium irradiance, LI low irradiance, FW full water, MW medium water, LW low water
a

Sky conditions: day 0 was cloudy and days 36 and 72 were clear days

domain reflectometry (TDR, MPKit-B, China) (Table 1).


Air temperature, relative humidity and soil temperature
were also measured at 1700 hours (Table 1). All measurements had six repetitions for each plot and each time.
Physiological traits measurements
In mid-September 2006, fully expanded sun leaves from
six to eight individuals of each species were selected for
gas exchange measurement. Light response curves were
made with a Li-6400 portable photosynthesis system (LiCor). Photosynthetic active radiation (PAR) was obtained
by using a quartz halogen light unit coupled to a leaf
chamber following the order 1,200, 1,000, 800, 500, 300,
200, 120, 50, 20, 0 l mol m-2 s-1 under fixed [CO2] at
380 l mol mol-1, leaf temperature 30 1C, air humidity
6070%, and vapor pressure deficit (VPD) 2.0 0.5 k Pa.
The Pmax was calculated by the nonrectangular hyperbola
model of Thornley (1976):

Pn

UI Pmax 

q
UI Pmax 2 4hUIPmax
2h

 Rd

where Pn is the photosynthetic rate (lmol CO2 m-2 s-1);


I is PAR (lmol photons m-2 s-1); U is the apparent
quantum yield (mol CO2 mol-1 photons); Pmax is the
maximum light saturated photosynthetic rate (lmol
CO2 m-2 s-1); Rd is the dark respiration rate (lmol
CO2 m-2 s-1); and h is the bending degree or curvature.
The light compensation point (LCP) was calculated when
the photosynthetic rate approached zero, and the light
saturation point (LSP) was calculated as the lowest value
of PAR for which photosynthesis reached 90% of Pmax.
Parameters of the model were calculated by the nonlinear
estimation module of SPSS 13.0 for windows (SPSS,
Chicago, IL).
Using the formula, by definition, Pmax is obtained at
infinite light intensity, so, in fixed 1,200 lmol m-2 s-1 PAR
we tested stomatal conductance (gs, mol H2O m-2 s-1), the

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ratio of intercellular to external CO2 concentration (Ci/Ca),


photosynthetic rate (A, lmol CO2 m-2 s-1) and transpiration rate (E, mmol H2O m-2 s-1). Intrinsic WUE
(lmol CO2 mmol H2O-1) values were calculated as A/gs for
each measurement (Pearcy et al. 1989), and PNUE as photosynthetic rate per mass (Amass)/N concentration (Field and
Mooney 1986).
Structural traits measurements
Seventy-five days after treatment application (9 October
2006), 30 fully expanded leaves were selected from separate plants of each treatment per species for SLA
determination with a portable laser leaf area instrument
(CID-203, Li-Cor), and then harvested and oven-dried at
65C to constant weight for calculating the SLA. Thereafter, ten plants for each treatment per species were
harvested and separated into samples of leaves, stems and
roots. Each sample was oven-dried to constant mass and
weighed to calculate leaf mass fraction (LMF), stem mass
fraction (SMF) (Poorter 1999) and the RGR. The ovendried leaf samples were ground for determination of N
concentration using an elemental analyzer (Quick Chem
FTA 8000 Series, Lachat, Loveland, CO).

Net photosynthetic rate


-2 -1
( mol CO2 m s )

(a) 20

At the beginning of treatment (time t1), ten plants per


species were harvested, oven-dried to constant mass and
weighed to determine initial weight W1. RGR was calculated as:
RGR ln W2  ln W1 =t2  t1

W2 being the dry mass after 75 days treatment (time t2)


(Radford 1967; Yamashita et al. 2002).
The level of response to variations in light (Responselight) and water (Responsewater) was estimated
according to Quero et al. (2006), and the index of
response was calculated according to Valladares et al.
(2000) as:
Response maximum value  minimum value=
maximum value

Statistical analyses
The samples collected were random and all parameters of
leaf physiological and structural characters were used to
test the differences between species and the effects of light
and water treatments on each variable by three-way analysis of variances (ANOVAs) (species, light and water as
source factors) with Type III sums of squares (Quero et al.

M. micrantha -FI
M. micrantha -MI

M. micrantha -LI

C. odorata -MI

C. odorata -LI

16
12
8

FW
MW
LW

4
0
-4

Net photosynthetic rate


-2 -1
( mol CO2 m s )

(b) 20

C. odorata -FI

16
12
8
4
0
0
-4

200 400 600 800 100 120 140


0
0
0

200 400 600 800 1000 1200 1400

200 400 600 800 1000 1200 1400

-2 -1

PAR (mol photons m s )


Fig. 1 Light response curves at various combinations of light and
soil water treatments. a Mikania micrantha, b Chromolaena odorata.
Light levels: full (100%, FI), medium (2535%, MI) and low (35%,
LI) irradiance, respectively. In each light condition, seedlings were

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under full (7090%, FW, closed diamonds), medium (3555%, MW,


open squares) or low (no watering, LW, open triangles) field water
capacity. Error bars SE of the mean (n = 6)

J Plant Res (2009) 122:6979

73

2006). All data were subjected to ANOVA, and means


were compared using the appropriate Fishers protected
LSD (P \ 0.01). Before ANOVA, data were checked for
normality and homogeneity of variances, and were logtransformed to correct deviations from these assumptions
when needed (Zar 1999). For correlation analysis of some
physiological and structural traits, we set separated and
integrated Spearmans analysis for both weeds depending
on light and water. All statistical analyses were performed
using SPSS 13.0 for windows (SPSS).

Results
General effects of light and water
The reduction in the availability of light and water imposed
structural changes on the leaves of both species and
affected their physiological performance (Fig. 1, Table 2).
Most variables showed strong light effects and were species-dependent (Table 2). In comparison, the effects of dry

conditions were far less obvious than those of light. Certain


effects of water and light interactions were also observed,
which were particularly significant in leaf area, SLA, LMF,
SMF and PNUE.
Leaf physiological traits and their differences
between species
Differences in physiological features between species
among various light and water treatments are displayed in
Figs. 1, 2, and Table 2. From FW to LW at FI, Pmax
declined significantly by 21.1% in M. micrantha but
increased by 22.3% in C. odorata. Pmax for both species
differed significantly between all light treatments under the
same water condition (Fig. 2a,b). WUE for both species
had a similar changing trend in that it declined from FI to
MI, and then increased under LI, which was particularly
evident for M. micrantha (Fig. 2c,d). Though variations in
Nmass were not significant among most treatments, PNUE
was markedly reduced as the result of Pmax attenuation at
lowered light availability (Fig. 2gj).

Table 2 Results of three-way ANOVAs for some structural and physiological traits, according to the treatment factors species (S), light (L) and
water (W)
Factor

R2

Interactions

Species

Light

Water

21.7***

42.2***

0.9***

S9L

S9W

L9W

S9L9W

3.4***

6.4***

1.4***

Structural traits
Area (cm2)
2

-1

SLA (cm g )

14.3***

6.3***

82.2

74.2***

0.7***

1.2***

0.7***

0.7***

1.0***

92.3

24.7***

3.7***

28.3***

1.0

5.6***

5.5***

69.0

16.5***

1.5*

25.1***

1.8*

5.4***

5.1***

65.1

62.2***

0.0

3.8***

1.2*

2.4**

2.3**

72.3

5.0**

16.2***

1.0

4.0*

3.0

53.1

5.5*

1.1

28.6***

54.6***

0.6

LMF (g g-1)

0.1

SMF (g g-1)

9.7***

RGR (g g-1 day-1)

0.2

Nmass (mg g-1)

4.6***

19.3***

Physiological traits
U (mol CO2 mol-1 photons)

0.4

h ()

14.2***

LCP (lmol photons m-2 s-1)

14.0***

LSP (lmol photons m-2 s-1)


Rd (lmol CO2 m-2 s-1)

1.8***
25.3***

3.5
79.2***
10.1***

0.3

4.7*

16.6***

0.0
3.3*

0.0
9.2***

5.2*

4.5

5.3

50.5

1.7

0.9

8.4***

80.7

4.9*

3.2

5.7*

52.6

2.9***
0.6

2.7**
0.3

3.0***
6.6*

89.5
55.4

Pmax (lmol CO2 m-2 s-1)

1.8***

89.7***

0.0

0.6***

0.5**

0.2

1.8***

94.6

WUE (lmol CO2 mmol H2O-1)

0.2

56.0***

2.8**

7.4***

1.2

2.4

7.1***

80.4

Ci/Ca

2.0**

56.3***

3.2***

12.1***

3.5***

2.7**

4.0**

83.7

gs (mol H2O m-2 s-1)

5.1***

76.7***

2.5***

2.9***

1.2***

3.5**

3.0***

94.8

PNUE (lmol CO2 (mol N)-1 s-1)

1.6***

78.8***

1.2***

4.9***

0.4*

1.9***

7.5***

96.2

The proportion of the explained variance (SS9/SStotal) and the level of significance for each factor and the interactions are indicated. R2 is the
proportion of total variance absorbed by the model. Area Single leaf area, SLA specific leaf area, LMF leaf mass fraction, SMF stem mass
fraction, RGR relative growth rate, Nmass nitrogen concentration, U apparent quantum yield, h bending degree or curvature, LCP light
compensation point, LSP light saturation point, Rd dark respiration rate, Pmax maximum light saturated photosynthetic rate, WUE water use
efficiency, Ci/Ca ratio of intercellular to external CO2 concentration, gs stomatal conductance, PNUE photosynthetic nitrogen-use efficiency
* P \ 0.05; ** P \ 0.01; *** P \ 0.001

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20

M . micrantha

(a)
Aa
BaBa

15

Ab Ab
Ab

10

C . odorata

(b)

Ba
Ba
Aa

FW
MW
LW

Ab
Ab Ab
Ac
AcAc

Ac
Ac Ac

Area (cm2)

Pmax ( mol CO2 m-2 s-1)

25

210
180
150
120
90
60
30
0

Ab Ac

(c)
Ba
Aa Aa

1200
Ac(d)
Ab

Aa
Aa
Aa
Aab

Ab
Aa Ab

Ab
Ab

Ba Aa

SLA (cm2 g-1)

(mmol H2O)-1)

WUE ( mol CO2

90
80
70
60
50
40
30
20
10
0

1000
800
600

M . micrantha

(a)

C . odorata
FW
MW
LW

Aa
AbAa
Ab
Ba
Ca

(b)

Ba
Aa

Ca

Ba
Bb
Ab t

Ab

Ac

Bb

AcAbAc

(c)

Ac Ac
Bb

Aa
Aa Ab
Aa

(d)

Ac

Bb

Ac
Bc Bc

Ab
Bb Cb

Aa
Aa Aa

400
200

Nmass (mg g-1)

60
50
40

(e)Aa

0.7

(f)
Ab Ab

0.6

Aa

Aa
Aa Aa Aa Ab
Bb

Ba

Ab Ac
Ac

AbAcAb

LMF(g g-1)

Aa

(g)

Aab
AbBbAb
Ba
Ab Aab
Aa Ba

Aa
Aa Aa

AbAaAa

20
10

Aa (i)

Ab
Ab
Ab

(f)
Aa Aa
Aa

Bab Bb Aa Bc
Aa
Aa

0.7
0.6
0.5
0.4
0.3
0.2
0.1
0.0
0.05

BaBa

Ab
Ab Aa

AaBa

Ca
Aa Aa Ab
Ab
Ab
Ac

200
AcAc Ab

100
0
FI

(g)Aa Aa Aa Aa Aa
Aa

(h)

AbAb
Ab

Aa
Aa
Aa Aa AaAaAab Aa
Bb

(j)

400

MI

LI

FI

MI

LI

RGR (g.g-1d-1)

PNUE ( mol CO2 (molN)1 -1


s )

300

0.4
0.3
0.2

Aa Aa
Aa

(h)

AB a
Aa Ba

30

500

0.5

(e)
Aa Aa
Aa

0.1
0.0

SMF(g g-1)

gs (mol H2O m-2s-1)

0
0.35
0.30
0.25
0.20
0.15
0.10
0.05
0.00

0.04
0.03

(i)

0.02

Ab Ab
Bc
Ab

0.01

(j)

AaAa Aa

Aa
Aa
Aa
Aa
AbAa

Ab

Ba
Ac
Ac Ac

Fig. 2 General variation in leaf physiological traits and Nmass of M.


micrantha (a, c, e, g, i) and C. odorata (b, d, f, h, j) under various
light and soil water conditions. a, b Pmax (maximum light saturated
photosynthetic rate; lmol CO2 m-2 s-1). c, d WUE (water use
efficiency; lmol CO2 mmol H2O-1). e, f gs (stomatal conductance;
mol H2O m-2 s-1). g, h Nmass (nitrogen concentration; mg g-1). i, j
PNUE [photosynthetic nitrogen-use efficiency; lmol CO2 (mol N)-1 s-1]. Different upper case letters Differences between
water treatments at the same light condition, different lower case
letters differences between light treatments at the same water
condition according to Fishers LSD tests at the confidence level of
P \ 0.01. Error bars SE of the mean (n = 6)

FI

MI

LI

FI

MI

LI

Fig. 3 General variation in leaf structural traits of M. micrantha (a, c,


e, g, i) and C. odorata (b, d, f, h, j) in response to the combination of
light and soil water conditions. a, b Area (single leaf area; cm2). c, d
SLA (specific leaf area; cm2 g-1). e, f LMF (leaf mass fraction;
g g-1). g, h SMF (stem mass fraction; g g-1). i, j RGR (relative
growth rate; g g-1 day-1). Different upper case letters Differences
between water treatments at the same light condition, different lower
case letters differences between light treatments at the same water
condition according to Fishers LSD tests at the confidence levels of
P \ 0.01. Error bars SE of the mean (n = 30 for area, SLA, and
n = 10 for the other parameters)

Structural traits and their differences between species


Leaf area, SLA and RGR were strongly influenced by light
availability and differed between species (Fig. 3, Table 2).
For example, irrespective of water treatment, from FI to LI,

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single leaf area and RGR decreased by 65.7 and 62.7% in


M. micrantha, and by 54.2 and 84.2% in C. odorata
(Fig. 3a,b,i,j), respectively; while SLA increased by 86.7
and 83.9% in M. micrantha and C. odorata, respectively

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(Fig. 3c,d). LMF and SMF were less affected by the varied
light and water interactions, particularly in C. odorata
(Fig. 3eh). Under the same light level, most structural
variables for both species did not vary significantly with
different water treatments (Fig. 3). Under LI, both species
had increased RGR with increasingly dry conditions, a
trend that was particularly significant for M. micrantha
(Fig. 3i, j).

(Fig. 5a, b). Amass values were positively and significantly


correlated with PNUE (Fig. 5e, f). Pmax values were negatively correlated with SLA under all water treatments
(Table 3). The correlations of WUE with most other variables were not statistically significant under all cases of
water treatment (Table 3).

Discussion
Response to variation of light and water
The response of both species to light (Responselight) was
generally higher than their response to water (Responsewater) (Fig. 4). Responselight in M. micrantha had a mean
value of 0.571 for the structural traits variables, which was
higher than that in C. odorata (Responselight = 0.533).
Conversely, the mean Responselight for the physiological
traits was 0.739 in M. micrantha, lower than that in
C. odorata (Responselight = 0.792). In particular, RGR of
C. odorata was strongly affected by light (Responselight = 0.989), suggesting that high light favored growth of
C. odorata. Both species showed the lowest response to
light and water in Nmass (Fig. 4).
Relationships between structural
and functional variables
The relationships between leaf structural and physiological
variables were similar for the two invasive weeds, with
integrated results shown in Table 3 and some separated
results in Fig. 5. The results indicated that most of the
correlations between structural and physiological variables
in both species did not change significantly with light
variance (data not shown). In most cases, the correlation of
structural traits with leaf physiological performance differed depending on water treatment (Table 3, Fig. 5).
Photosynthetic rates on a mass basis (Amass) were significantly correlated with RGR under FW and MW for M.
micrantha, and under all water treatments for C. odorata

C.odorata

M. micrantha

1.0

Structural
Physiological

0.8

1.0
RGR

Rd

LCP

0.8

0.6

LSP

Ci/Ca
WUE

Rd

0.4

PNUE

SLA

Pmax

SMF LMF

0.2

Response water

gs

0.0

RGR

Area

0.6

LCP
gs

Ci/Ca
SLA

0.4

WUE
LMF

PNUE

Pmax

SMF

Nmass

0.2

Nmass

LSP

Area

Response water

Fig. 4 Bivariate diagram of the


comparative response to light
(Responselight) versus water
(Responsewater), for structural
and physiological traits of
M. micrantha and C. odorata.
Response was calculated as
(maximum value - minimum
value)/maximum value

Our study showed that the impacts of light treatment on the


structural and physiological traits of both species were
generally more pronounced than those of soil water treatment. Both weeds had significantly higher Pmax under high
light than low light (Fig. 2a,b,e,f), confirming that
increasing photosynthesis in high light could help invasive
plants achieve success (Baruch and Goldstein 1999). Plants
with a low SLA will have higher N per leaf area, under a
given N concentration. In the present study, leaf N on a
mass basis tended to be constant, especially in C. odorata,
but the results for PNUE were generally consistent with
Pmax and negatively correlated with SLA in both species,
indicating that higher N per leaf area should translate into
higher photosynthetic capacity under high light in spite of a
low SLA. These findings are in contrast with the results of
other studies examining the relationship among Pmax, leaf
N and SLA across species, which indicated that species
with low SLA generally had a lower PNUE and a smaller
change in Pmax per leaf N (Field and Mooney 1986; Reich
and Walters 1994). However, our results are consistent
with those of McDowell (2002) on invasive species of
Rubus, which showed that invasive species may have different combinations of leaf traits than plants considered
noninvasive species.
Under high light, Pmax and RGR showed decreasing
trends in M. micrantha but increasing trends in C. odorata
with soil water reduction. No significant differences in
Pmax or RGR were observed between MW and LW in C.
odorata under high light, but single leaf area significantly

0.0
0.0

0.2

0.4

0.6

Response light

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

Response light

123

76

J Plant Res (2009) 122:6979

Table 3 Spearmans correlation coefficients for some log structural and physiological traits at three different water treatments on integrated data
from both weeds
Pmax

gs

PNUE

Nmass

SLA

RGR

LMF

SMF

WUE

LSP
FW

0.94**

0.89*

0.83*

-0.49

-0.89*

0.89*

-0.49

0.38

-0.37

MW

0.60

0.60

0.54

-0.14

-0.60

0.54

-0.54

0.37

-0.83*

LW

0.94**

0.60

0.77

-0.54

-1.00**

0.94**

-0.52

0.43

0.89*

WUE
FW

-0.31

-0.49

-0.49

0.14

0.20

-0.14

0.83*

-0.83*

MW
LW

-0.43
-0.49

-0.68
-0.83*

-0.49
-0.37

0.26
0.60

0.43
0.60

-0.37
-0.54

0.60
0.77

-0.37
-0.71

FW

0.2

0.41

0.26

-0.64

-0.06

0.03

-0.99**

MW

0.09

0.54

0.37

-0.77

-0.09

-0.03

-0.94**

LW

0.54

0.89*

0.66

-0.89*

-0.43

0.49

-0.93**

-0.14

SMF

LMF
FW

-0.31

-0.54

-0.37

0.66

0.14

MW

-0.26

-0.60

-0.43

0.83*

0.26

-0.09

LW

-0.67

-0.90*

-0.70

0.99**

0.52

-0.46

RGR
FW

0.83*

0.83*

0.66

-0.14

-0.89*

MW

0.94**

0.71

0.89*

-0.09

-0.94**

LW

0.89*

0.54

0.83*

-0.49

-0.94**

SLA
FW
MW

-0.94**
-1.00**

-0.66
-0.66

-0.83*
-0.83*

0.14
0.31

LW

-0.94**

-0.60

-0.77

0.54

Nmass
FW

-0.31

-0.37

-0.20

MW

-0.31

-0.43

-0.37

LW

-0.71

-0.83*

-0.77

PNUE
FW

0.94**

0.71

MW

0.83*

0.94**

LW

0.89*

0.54

gs
FW

0.77

MW

0.66

LW

0.66

See Table 2 for abbreviations


* P \ 0.05, ** P \ 0.01, *** P \ 0.001

decreased in LW compared to MW, indicating that, under


high light, M. micrantha favored FW, and LW limited the
growth of C. odorata to a certain extent, though it seemed
to perform better in LW than in FW conditions. This
result supported the finding of Vanderwoude et al. (2005)
that C. odorata grew poorly when relative soil water
content exceeded 80%. However, the latter study did not
consider the effects of light treatments, and we further
found that C. odorata could perform better in as low as

123

3.7% compared to 90% relative soil water content under


high light.
Shade significantly reduced most of the structural and
physiological variables of both species. In fact, over half of
M. micrantha individuals died under LI, which occurred
beginning in mid-September and first occurred for the FW
treatment, then MW and finally LW. However, C. odorata
survived all treatments, although RGR significantly
decreased with light reduction. These results are in

J Plant Res (2009) 122:6979

77

M . micrantha

C . odorata

A mass (nmol CO2 g-1 s-1)

1200

(a)

1000

(b)

800
600
400
200

FW: r=0.79**

FW: r=0.50*

MW: r=0.84**

MW: r=0.77**

LW: r=0.40ns

LW: r=0.86**

0
0

0.02

0.04

0.06

0.02

0.04

0.06

RGR (g g-1d-1)

RGR (g g-1d-1)

RGR (g g-1 d-1)

0.05

(c)

0.04

(d)

FW: r= - 0.83**

FW: r= - 0.87**
MW: r= - 0.87**

MW: r= - 0.88**

LW: r= - 0.83**

LW: r= - 0.63**

0.03
0.02
0.01
0

400

800

1200

1600

400

SLA (cm 2 g-1)

800

1200

1600

SLA (cm2 g-1)

(f)

(e)

400

(mol N)-1s-1)

PNUE (mol CO2

500

300
200
100

FW: r=1.00**

FW: r=0.95**

MW: r=0.99**

MW: r=0.97**

LW: r=1.00**

LW: r=1.00**

0
0

500

1000

1500

A mass (nmol CO 2 g-1 s-1)

2000

500

1000

1500

2000

A mass (nmol CO 2 g-1 s-1)

Fig. 5 Correlations between leaf traits in M. micrantha (a, c, e) and


C. odorata (b, d, f). a, b Photosynthetic rate on mass basis (Amass).
c, d specific leaf area (SLA) versus relative growth rate (RGR).
e, f Photosynthetic nitrogen-use efficiency (PNUE) versus Amass

accordance with previous reports that M. micrantha died


under 2% irradiance (Kuo et al. 2003) whereas C. odorata
could survive under 4% irradiance (Wang et al. 2003).
Growth at low light, or switching plants from high to
low light, generally causes an increase in SLA, due to a
significant increase in leaf area (Evans 1972), which may
be a way of improving the plants ability to assimilate CO2
under shaded conditions (Monaco et al. 2005). Our results
showed that both species compensated for low light primarily through modifying structural traits, such as by
achieving higher SLA even though leaf area significantly
decreased under shade conditions relative to FI (Fig. 3ad).
These findings suggested that both species were unable to
achieve larger leaf area to capture more light under high
shade conditions. Additionally, decreases in leaf dry mass
were higher than reductions in leaf area, implying that both
species failed to achieve abundant leaf biomass under
shade, especially the shade extremes, as well confirmed by
field survey data showing that the access and invasibility of
these weeds into deep shade habitats such as dense forests
is very limited (Huang et al. 2000).

Plant growth is directly influenced by the allocation of


biomass between leaves and stems (Evans 1972; Reich
et al. 1998) and RGR is enhanced by high LMF because it
confers high carbon gain per unit mass invested in leaves
(Poorter and Remkes 1990). Our results show that deep
shade caused an increase in LMF and a decrease in SMF
for M. micrantha under all water treatments, while in C.
odorata both fractional ratios were similar and nearly
consistent among all treatments except the LILW combination (Fig. 3eh). It appears that one way for M.
micrantha to enhance growth under shade is by increasing
allocation of biomass to leaves. In contrast, C. odorata
seems to allocate a certain percentage of carbon to stems to
sustain mechanical stability under most light and soil water
conditions, which might partially explain its biological
form as an herbaceous shrub.
Holmgren (2000) proposed that, when subjected to
drought stress, plants under high light suffer a more drastic
reduction in CO2 assimilation rate, and could be more
predisposed to photoinhibition, as compared with plants
under shade conditions. In the present study, dry conditions
at LI did not result in significant reduction of Pmax and
PNUE, while leaf area, RGR and gs increased with
increasingly dry conditions for both species (Figs. 2, 3),
suggesting that shade did not aggregate the drought
impacts on the two weeds. This was consistent with the
results of other studies that shading could lessen drought
stress on some plants (Holmgren 2000; Quero et al. 2006).
Leaf structural and physiological traits differed in
response to light and water treatments in both species
(Fig. 4). For example, high light induced a relatively high
variation in the key leaf trait Pmax for both species (mean
Responselight = 0.87), indicating their adaptation to high
irradiance. The measured Responsewater for structural traits
in M. micrantha were higher than those in C. odorata
(Fig. 4), indicating that drought induced greater effects on
structural traits of M. micrantha than of C. odorata.
In some cases, leaf structural traits are good predictors
of plant physiological performance (Quero et al. 2006).
Our study showed that SLA was negatively correlated with
RGR and Pmax at all water treatments (Table 3, Fig. 5c, d),
suggesting that SLA was a good predictor of Pmax
(Table 3), and the high negative correlations between Pmax
and SLA were in line with a suggested buffering of RGR
due to a trade-off between photosynthetic rate and SLA
(Poorter 1989).

Conclusions
The results presented here indicate that both species favor
high light conditions, while differing in their soil water
preferences: M. micrantha was particularly efficient at full

123

78

soil water regimes and C. odorata at moderate soil water


conditions. Limited light availability under extreme shade
restricted the growth of both weeds, particularly M. micrantha. The high structural and physiological plasticity in
response to high light and favored soil water status may
improve the growth advantages that benefit their invasion.
When satisfied with the gross climate requirement, M.
micrantha is most likely to invade well-lit and wet sites,
while C. odorata has the potential for expansion and
invasion at high light and moderate or even low soil water
regimes. Moreover, both species had the lowest structural
and physiological plasticity in deep shade, implying that
shade by intact canopies would be an effective barrier
against invasion by both weeds in the field.
Acknowledgments We gratefully acknowledge Ms. Fang-Fang Sun
(Ph.D.) and Mr. En-Qing Hou (M.Sc.) for their assistance in field
work and in the laboratory. This study was financially supported by
National Natural Science Foundation of China (Project No.
30630015) and the Pearl River Delta Urban Forest and the Environment Research Programme of SCBG.

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