Comparison of ecophysiological characteristics between introduced and indigenous mangrove species in China

Estuarine, Coastal and Shelf Science 79 (2008) 644–652

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Comparison of ecophysiological characteristics between introduced and indigenous mangrove species in China Luzhen Chen a, b, f, Nora F.Y. Tam b, c, Jianhui Huang a, Xueqin Zeng a, b, e, Xiangli Meng a, e, Cairong Zhong d, Yuk-shan Wong b,1, Guanghui Lin a, f, * a

State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, China Futian-City University Mangrove R&D Center, Shenzhen 518040, China Department of Biology and Chemistry, City University of Hong Kong, Hong Kong d The Administrative Bureau of Dongzhai Harbor National Nature Reserve, Haikou 571129, China e Graduate School of Chinese Academy of Sciences, Beijing 100049, China f Key Laboratory for Subtropical Wetland Ecosystem Research, Ministry of Education and School of Life Sciences, Xiamen University, Xiamen, Fujian 361005, China b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 7 April 2008 Accepted 5 June 2008 Available online 11 June 2008

Due to its rapid growth, the introduced mangrove species Sonneratia apetala from Bangladesh has been widely used in mangrove restoration in southeastern China since 1985. As an indigenous mangrove species in Hainan, China, Sonneratia caseolaris was also planted in Guangdong Province for afforestation purposes. Both species have developed well in their new habitats, but their ecophysiological differences with the native mangrove species have not been studied. In this study, leaf gas exchange, water and nitrogen use efficiencies of two Sonneratia species were compared with those of selected native mangrove species (Avicennia marina, Aegiceras corniculatum, Kandelia candel, and Excoecaria agallocha) in Hainan and Shenzhen. The introduced S. apetala maintained lower carbon assimilation rate (A) and photosynthetic nitrogen use efficiency (PNUE) than the indigenous S. caseolaris. In Shenzhen, the two introduced Sonneratia had comparable photosynthetic rates and water use efficiency (WUE) with the native mangrove species, except that PNUE in S. caseolaris was significantly higher than in the native mangrove species. The two Sonneratia species showed significant overlap in PNUE and long-term WUE. Photosynthetic parameters derived from leaf photosynthetic light–response curves and A–Ci curves also suggested lower carbon assimilation capacities for the introduced Sonneratia than for the native mangrove species in both study sites. The lower light compensation point (LCP) of two introduced Sonneratia in both study sites also indicated a better adaptation to a low light regime than the native mangrove species. The results of photosynthetic capacities indicated that the introduced mangrove species have little competitive advantage over local native mangrove species in their respective new habitats. Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: mangroves Sonneratia gas exchange d13C value alien species competition

1. Introduction It is well known that exotic plants have invaded different ecosystems all over the world (Drake et al., 1989; Higgins and Richardson, 1996). An invasive exotic species can spread very fast, become out of control in a new environment, and occupy the ecological niches of indigenous species. They can also compete with indigenous species for resource and habitat, which can threaten the survival of indigenous species (Drake et al., 1989). Exotic species are

* Corresponding author. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, the Chinese Academy of Sciences, Beijing 100093, China. E-mail address: [email protected] (G. Lin). 1 Present address: The Hong Kong University of Science and Technology, Hong Kong. 0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.06.003

often used for restoration and afforestation purposes because of their fast growth rates. For example, Sonneratia apetala has frequently been used in mangrove restoration programs to produce a ‘‘green wall’’ along the coastline in China (Liao et al., 2004). Sonneratia apetala was originally introduced from the Sundarbans, southwest of Bangladesh in 1985 to Dongzhai Harbor Mangrove Nature Reserve (Hainan Province, China). This species developed well and started to produce flowers and fruits three years after the introduction (Wang and Zheng, 1992). In October 1998, 13 years after the first introduction, the tallest individual of S. apetala reached a height of 13.5 m in Dongzhai Harbor (Wang et al., 2002). Since then, S. apetala has been extensively used in many mangrove planting programs in China. Another mangrove species commonly planted in the coastal areas of China is Sonneratia caseolaris, one of the five indigenous Sonneratia species in Hainan Province (Ko, 1985). It was first introduced to Futian Mangrove Nature Reserve

L. Chen et al. / Estuarine, Coastal and Shelf Science 79 (2008) 644–652

(Shenzhen, Guangdong Province) in 1993 as an afforestation species (Fig. 1). As an introduced species, S. caseolaris grew very fast in Shenzhen and formed a dense community (Wang et al., 2002). Sonneratia species are well suited for mangroves restoration because they can be planted in low inter-tidal zones where other indigenous species are unable to colonize (Liao et al., 2004). In addition to their fast growth rates, their high tolerance to environmental stresses was also considered to enhance their success in mangrove restoration projects (Li et al., 1997; Liao et al., 2004). With the success in the establishment and fast growth of Sonneratia in new habitats, their potential invasiveness has become of increasing concern. Previous studies have called for special attention to the possible impact of introduced plants that have unproven invasion potentials (Forman, 2003). A heated debate has ensued in China to whether these two Sonneratia species should be planted or not (Ding and Xie, 1996; Liao et al., 2004). Invasive plants often have higher gas exchange rates than the indigenous species (Pattison et al., 1998; Baruch and Goldstein, 1999; Durand and Goldstein, 2001; Ewe and Sternberg, 2003). Several studies have investigated characteristics of the exotic mangroves species that have either been introduced or have become naturalized (Allen, 1998; Allen et al., 2000; Krauss and Allen, 2003). Higher leaf gas exchange rates are often attributed to the competitive nature of introduced species in non-native habitats (Drake et al., 1989). Water-use efficiency (WUE) and nitrogen-use efficiency (PNUE) are also important factors that contributed to plant growth and resource capture (Patterson et al., 1997; Chen et al., 2005). Mangroves with lower dark respiration rate (Rday) and light compensation point (LCP), but higher apparent quantum yield (FCO2) have shown to be better adapted to low light regime (Krauss and Allen, 2003). Although the introduced Sonneratia apetala has better growth than the indigenous mangrove species in China (Zan et al., 2003), the differences in their photosynthetic performance and nutrient accumulation mechanisms have not been studied previously. The present study therefore investigates leaf gas exchange characteristics and other ecophysiological factors of the introduced Sonneratia species in two different habitats, Futian in Shenzhen and Dongzhai Harbor in Hainan, in comparison with some common native mangrove species at each location. We tested the hypotheses that: (1) the introduced Sonneratia species has higher gas exchange rates than the native mangrove species; and (2) the introduced Sonneratia species has better adaptive strategies in photosynthetic capacities than the native mangrove species. Leaf gas exchange, carbon isotope ratios and leaf nitrogen contents were measured to evaluate the physiological patterns of the introduced Sonneratia mangrove species in China. Foliar carbon isotope ratio (d13C) is

25º N Shenzhen, Gongdong Province

China

Dongzhai Harbor, Hainan Province

20º N

105º E

110º E

115ºE

Fig. 1. Map of southern China showing the study sites. Two study sites are Shenzhen in Guangdong Province and Dongzhai Harbor in Hainan Province.

645

positively related with long-term WUE of plants during a growing season, which can provide a timely-integrated indication of photosynthetic performance and plant metabolism (Farquhar et al., 1989). The calculations of Amax, LCP, LSP and FCO2, Vc,max and Jmax from light–response curves and A–Ci curves were also essential in determining the photon utilization efficiency, photosynthetic capacity and carboxylation efficiency of the introduced and the native species in new habitats (Farquhar et al., 1980; Atkinson and Winner, 1987). 2. Materials and methods 2.1. Study sites and species The present study was carried out in two mangrove areas of southern China (Fig. 1). Dongzhai Harbor Mangrove Nature Reserve (19 540 N, 110 200 E) is near Haikou City, Hainan Province, while Futian Mangrove Nature Reserve (22 320 N, 114 050 E) is located in Shenzhen City, Guangdong Province. Both are important natural mangrove reserves in China and the mangroves in these locations represent typical natural mangrove communities under two different climate zones, tropical and subtropical climates, respectively. The basic characteristics of the two sites are summarized in Table 1. Sonneratia apetala is an exotic species and was introduced to Hainan from Bangladesh in 1985 and then to Shenzhen in Guangdong Province. Sonneratia caseolaris is an indigenous species in Hainan but has become an introduced mangrove species in Shenzhen since 1993. Thus, Shenzhen is considered as a new habitat for both Sonneratia species. Four indigenous mangrove species in Hainan and Shenzhen mangrove reserves, namely Kandelia candel, Aegiceras corniculatum, Avicennia marina and Excoecaria agallocha, were also chosen for the comparison. Except for A. corniculatum, which is a shrub species, the other mangrove species selected were tree species. All the mangrove trees for the measurements were selected from open-grown environments, and they were distributed in habitats of similar mid-to-high tidal level. During the measurement periods, the both study sites were no flooded. The salinity of sea water or soils at the study sites were about 10–15&. The soil organic matter contents were about 7.4–8.6% in the sample sites of Shenzhen and about 5.7–6.2% in the sample sites of Hainan, respectively, according to the method of Lu (2000). 2.2. Leaf gas exchange measurements Gas exchange of mature leaves was measured using a LI-6400 portable photosynthesis system (Li-Cor Inc., Lincoln, NE, USA) with a 6-cm2 clamp-on leaf cuvette. Measurements were made between 09:30 and 15:00 h in early November with day-time temperatures ranging from 25 to 28  C. The measurements were carried out at 1000 mmol photons m2 s1 light intensities and at an internal leaf cuvette CO2 concentration of 350 mmol m2 s1. For each mangrove species, including the introduced Sonneratia species (i.e. Sonneratia apetala in Hainan, S. apetala and Sonneratia caseolaris in Shenzhen) and the indigenous mangrove species (S. caseolaris, Kandelia candel, Aegiceras corniculatum, Avicennia marina, Excoecaria agallocha in Hainan; K. candel, A. corniculatum, A. marina, E. agallocha in Shenzhen), four mature, fully expanded second or third leaves from the top of branches, were chosen for the measurement of assimilation rate (A), transpiration rate (E), stomatal conductance (gs); and intercellular CO2 concentration (Ci) were measured by the LI-6400 system. For each mature leaf, five measurements were taken and the results were averaged as one replicate. The mean value of each species was calculated based on the four replicates of individual plants. Instantaneous water use efficiency (WUEi) of the sampled leaf was calculated according to the ratio of A/E.

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Table 1 Key environmental parameters for the native habitats and the two plantation sites of Sonneratia apetala and Sonneratia caseolaris (adapted from Li et al., 1997; Wang et al., 2002) Sites

Climate Zone

Latitude (N)

Mean annual temperature ( C)

The coldest month’s temperature ( C)

Mean annual rainfall (mm)

Annual length of day (h)

Seawater salinity

Sundarbans (Bangladesh)

Monsoonal tropical humid climate Tropical monsoon climate Subtropical monsoon climate

21310 –22 300

24.1

13.8

1690–1770

NDa

NDa

19 540 –20 010 22 320

23.8 22.0

17.2 14.1

1685 1927

2240 2209

21.9 <15.0

Dongzhai Harbor (Hainan, China) Shenzhen (Guangdong, China) a

ND, no data available.

Light–response curves of the two Sonneratia species and the indigenous Avicennia marina in both study sites were generated from the photosynthetic measurements using the same LI-6400 system coupled with a red-blue LED (light-emitting diode) light source. The measurements were carried out at 10 levels of PAR (photosynthetic active radiation) intensities (1600, 1200, 800, 400, 200, 100, 50, 20, 10 and 0 mmol photons m2 s1) in the sequence from the highest to the lowest values at 2 min intervals for each light intensity level, and made only after the leaf was equilibrium with a new light intensity. Four or five leaves of a tree were measured and averaged as one replicate, The mean value of each light intensities level of each species were calculated based on the three replicates of individual plants. All measurements were made at 350 mmol mol1 CO2 concentration. The ambient air temperature was 26–28  C and leaf temperature was 28–30  C. The apparent quantum yield (FCO2), maximum photosynthetic rate (Amax), light compensation point (LCP), and light saturation point (LSP) were calculated from each sample’s light response curve using Photosyn Assistant Software (Version 1.1, Dundee Scientific, UK) according to Long et al. (1993). All of these parameters can be determined by fitting data to the model function, expressed as a quadratic equation by Prioul and Chartier (1977).

A ¼

FCO2 Q þ

qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi ðFCO2 Q þ Amax Þ2 4FCO2 QkAmax 2k

 Rday

where A is net assimilation rate (mmol CO2 m2 s1), FCO2 the apparent quantum yield of CO2 (mol CO2 mol1 photons), Amax the maximum photosynthetic rate (mmol CO2 m2 s1), Q the light level (mmol m2 s1), k the convexity coefficient (0 < k < 1), and Rday the dark respiration rate in daytime (mmol CO2 m2 s1). A–Ci curve, where Ci is internal concentration of CO2, showing the relationship between net assimilation and CO2 partial pressure was examined over a range of 11 external CO2 partial pressures (Ca) from 0 Pa to 160 Pa. Measurement was made under artificial light intensity of 1000 mmol photons m2 s1, and ambient temperature 26–28  C and an ambient relative humidity of 53–67%. The maximum rate of carboxylation by Rubisco (Vc,max) and the PAR-saturated rate of electron transport (Jmax) were obtained from each A–Ci curve using the same Photosyn Assistant Software mentioned above. The program uses the modified photosynthesis model proposed by Farquhar et al. (1980). The leaves of the four native mangroves species except Avicennia marina in both study sites could not maintain full functions long enough for the measurements for the both light– response curves and A–Ci curves because they were too sensitive to the disturbances caused by such measurements, thus the data were not included in the final analyses. Three typical curves of both Sonneratia species and native A. marina were generated and analyzed. The mean values of Vc,max and Jmax of each species were calculated based on the three replicates of individual plants.

2.3. Field sampling and laboratory analysis Leaves for the gas exchange measurements were harvested after measurement. Leaf areas were measured using a LI-3000 area meter (Li-Cor Inc.). The leaves were washed in distilled water and then dried at 65  C for at least 48 hrs. The dried leaves were then ground using a mortar and pestle, passing a 20-mesh sieve, and used for stable isotope analysis. Carbon isotope ratios of the leaf samples were analyzed using a Thermo Finnigan MAT DELTAplus XP isotope-ratio mass spectrometer coupled with a Flash EA 1121 (Thermo Finnigan, Bremen, Germany). Carbon isotopic ratio, in per mil units (&), was expressed as in the following equation:

d13 C ¼



Rsample Rstandard



  1  1000

where Rsample was the 13C/12C ratio of the sample and Rstandard was the 13C/12C ratio of the Pee-Dee Belemnite standard. Leaf carbon isotopic signature was used as a proxy for integrated plant wateruse efficiency (WUE) as d13C values have been shown to be positively related to WUEi over its lifespan (Farquhar et al., 1982). Another sub-set of leaf samples were used for determination of total carbon and nitrogen concentrations. Leaf nitrogen content was expressed as g N m2 leaf. Photosynthetic N use efficiency (PNUE, mmol CO2 g1 N s1) was determined by dividing A by leaf nitrogen content (Ewe and Sternberg, 2003). 2.4. Statistical analyses Mean and standard error (S.E.) of four replicates were calculated for leaf gas exchange and d13C values, leaf N contents, and PNUE. Mean and standard error (S.E.) of three replicates were calculated for Amax, FCO2, LCP, LSP, Vc,max and Jmax from three species light– response and A–Ci curves. Leaf gas exchange, d13C values, leaf N contents, and PNUE among six species and Amax, FCO2, LCP, LSP, Vc,max and Jmax from three species light–response and A–Ci curves in each site were analyzed using one-way ANOVA following LSD test (least significant difference test). The introduced species (Sonneratia apetala in Hainan; S. apetala and Sonneratia coseolaris in Shenzhen) and native species in both study sites were also tested using one-way ANOVA. All the parameters of the six species in two study sites were analyzed by parametric two-factor multivariate analysis-of-variance (MANOVA) with power analysis. All analyzes were carried out using SPSS 11.5 (SPSS Inc., Chicago, IL). 3. Results 3.1. Physiological characteristics In Hainan, the introduced Sonneratia apetala had significantly lower A, leaf N content, WUEi and higher Ci than the indigenous Sonneratia caseolaris (Figs. 2A,G, 3A, 4A, and Table 2). A of S. caseolaris was nearly 1.38 times of that for the introduced S. apetala at the Hainan site. In Shenzhen, A, E, gs and PNUE were also

L. Chen et al. / Estuarine, Coastal and Shelf Science 79 (2008) 644–652

Hainan

Shenzhen

20

A (μmol m-2 s-1)

introduced

A

native species

b

15

introduced

ac

c

b

c

c

10

B

native species b

a ac

647

c

a d

5

0

E (μmol m-2 s-1)

a 3

C

a

b

D

b

ab

a b

b

ab

ac

b 2

c 1

0

E

a

a

gs (mmol m-2 s-1)

a

b b

.15

ab

c c a

.10

a

b .05

0.00 250

a

G

a b b

200

Ci (ppm)

F

b

ac

b

a

ac

ac

Ea

Sa

Sc

Am

bc

H

ac

b

150 100 50 0 Sa

Sc

Am

Ac

Kc

Ac

Kc

Ea

Fig. 2. Assimilation rate A (A, B), transpiration rate E (C, D), stomatal conductance gs (E, F), intercellular CO2 concentration Ci (G, H) of the two introduced Sonneratia species and the four indigenous mangrove species in Hainan and Shenzhen. Sa, Sonneratia apetala; Sc, Sonneratia caseolaris; Am, Avicennia marina; Ac, Aegiceras corniculatum; Kc, Kandelia candel; Ea, Excoecaria agallocha. Vertical bars indicate standard errors of the mean (n ¼ 4). Different letters represent significant differences between species in each study site (ANOVA with LSD test, p < 0.05).

significantly higher in S. caseolaris than S. apetala (Figs. 2B,D,F, 4D, and Table 2). For example, A of the introduced S. caseolaris was 1.67 times of that for S. apetala and its PNUE was almost 2 times of that for S. apetala in Shenzhen. As an introduced species in Hainan, Sonneratia apetala had similar A with most of the indigenous mangrove species except Sonneratia caseolaris (Fig. 4A, Table 2). Ci of the introduced S. apetala and the native Aegiceras corniculatum were the highest among all

measured mangrove species in Hainan (Fig. 2G, Table 2). The introduced S. apetala had significantly lower WUEi than the indigenous species expect A. corniculatum (Fig. 4A, Table 2). The introduced S. apetala in Hainan had the similar d13C value to the indigenous S. caseolaris and Avicennia marina, which was lower than Excoecaria agallocha but higher than A. corniculatum and Kandelia candel (Fig. 3C). Although the leaf N content for the introduced S. apetala was the lowest in Hainan, the PNUE of this

L. Chen et al. / Estuarine, Coastal and Shelf Science 79 (2008) 644–652

Leaf N content (g N m-2 leaf area)

648

Hainan

5 introduced

Shenzhen

A

native species

introduced

B

native species b

4 c

c

bc

c

3

c b

b

a

b

a

2

a

1

0 -22

δ 13C (‰)

-24 -26 c -28

c a

a

d

a

-30

b

b

b

C

a

a

b

D

-32 Sa

Sc

Am

Ac

Kc

Ea

Sa

Sc

Am

Ac

Kc

Ea

Fig. 3. Leaf N contents (A, B), and leaf d13C values (C, D) of the two introduced Sonneratia species and the four indigenous mangrove species in Hainan and Shenzhen. Sa, Sonneratia apetala; Sc, Sonneratia caseolaris; Am, Avicennia marina; Ac, Aegiceras corniculatum; Kc, Kandelia candel; Ea, Excoecaria agallocha. Vertical bars indicate standard errors of the mean (n ¼ 4). Different letters represent significant differences between species in each study site (ANOVA with LSD test, p < 0.05).

WUEi (μmol CO2 mmol H2O-1)

Shenzhen

Hainan

8 introduced

A

native species

B

native species

b bc

6

bc

a

ac

a

a

a

a

a

a

a

4

2

0

PNUE (μmol CO2 s-1 g-1N)

introduced

8

ac

D

C

a c

b

c

6 b

a

a

b

a

a

4

c 2

0 Sa

Sc

Am

Ac

Kc

Ea

Sa

Sc

Am

Ac

Kc

Ea

Fig. 4. Leaf instantaneous water use efficiency WUEi (A, B) and photosynthetic N use efficiency PNUE (C, D) of the two introduced Sonneratia species and four indigenous mangrove species in Hainan and Shenzhen. Sa, Sonneratia apetala; Sc, Sonneratia caseolaris; Am, Avicennia marina; Ac, Aegiceras corniculatum; Kc, Kandelia candel; Ea, Excoecaria agallocha. Vertical bars indicate standard errors of the mean (n ¼ 4). Different letters represent significant differences between species in each study site (ANOVA with LSD test, p < 0.05).

L. Chen et al. / Estuarine, Coastal and Shelf Science 79 (2008) 644–652

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Table 2 Significance values of one-way ANOVA (F) and multivariate analysis-of-variance (MANOVA) (F) for the comparisons in the key leaf physiological parameters between the introduced and the indigenous mangrove species for six species in two study sites in China. Sa, Sonneratia apetala; Sc, Sonneratia caseolaris. Levels of significance are shown as: *p < 0.05, **p < 0.01, ***p < 0.001 Comparison

df

A

Sa vs. Sc

Hainan Shenzhen

1, 6 1, 6

Introduced species vs. Native species

Hainan Shenzhen

1, 22 1, 22

Six species of multivariate analysis-of-variance (MANOVA)

Site Species Species  Site

E

21.168** 52.063*** 1.172 0.072

1 5 5

3.756 8.542*

gs

Ci

Leaf N content

0.857 57.522***

6.652* 0.141

11.96* 0.687

0.389 0.342

5.662* 3.252

3.045 2.882* 1.004

0.122 3.126* 2.595*

0.096 0.465

66.451*** 28.341*** 9.221***

0.453 12.515*** 3.750**

WUEi

PNUE

0.628 1.627

3.683 0.646

0.797 31.838***

8.319** 16.478**

0 15.444**

3.825 0.172

2.618 13.655**

11.453** 20.251*** 2.156

29.617*** 71.761*** 35.969***

10.229** 4.180** 0.591

88.174*** 45.197*** 4.711**

corniculatum (Fig. 4F). In addition, these introduced species in Shenzhen had the lowest leaf d13C values, leaf N contents among all species in Shenzhen (Fig. 3D, Table 2), but S. caseolaris the highest PNUE in Shenzhen (Fig. 4D, Table 2).

species was significantly higher than the native A. marina and K. candel (Figs. 3A, 4C). The introduced S. apetala had significantly lower leaf N content and higher Ci than the average of all measured indigenous species in Hainan (Table 2). As an indigenous in Hainan but introduced species in Shenzhen, Sonneratia caseolaris had significantly higher A than another introduced species Sonneratia apetala and the indigenous species except Avicennia marina (Fig. 2B). For the introduced S. apetala, however, A was significantly lower than all native species in Shenzhen except Kandelia candel (Fig. 2B). Both introduced Sonneratia species showed different leaf N content, d13C values and PNUE from all native species tested at the Shenzhen (Table 2), but had similar gs to those of the indigenous A. marina and Aegiceras

3.2. Light–response curves and A–Ci curves The typical shapes of light–response and A–Ci curves of both Sonneratia species and Avicennia marina growing in both study sites are shown in Fig. 5. Photosynthetic characteristics including Amax, FCO2, LCP and LSP derived from the light–response curves were shown in Table 3. As the indigenous species in Hainan, Sonneratia caseolaris and A. marina had significantly higher Amax,

Sa Sc Am

Hainan

d13C

25

Sa Sc Am

Shenzhen

A

B

A (μmol CO2 m-2 s-1)

20 15 10 5 0 -5 0

500

1000

0

1500

500

1000

1500

PPFD (μmol photon m-2 s-1) 50

D

C

A (μmol CO2 m-2 s-1)

40 30 20 10 0 -10 0

20

40

60

80

100

120

140

0

20

40

60

80

100

120

140

Ci (Pa) Fig. 5. Typical light–response curves (A, B) and A–Ci curves (C, D) of the two introduced Sonneratia species and the native Avicennia marina in Hainan and Shenzhen. Sa, Sonneratia apetala; Sc, Sonneratia caseolaris; Am, Avicennia marina. (n ¼ 3).

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Table 3 Mean photosynthetic parameter values (  standard error) estimated from the light–response curves and A–Ci curves, and significance values of multivariate analysis-ofvariance (MANOVA) of three mangrove species in two study sites in China Amax (mmol m2 s1)d

FCO2 (mol CO2 mol1)e

LCP (mmol m2 s1)f

LSP (mmol m2 s1)g

Vc,max (mmol m2 s1)h

Jmax (mmol m2 s1)i

Hainan

Saa,j Scb,j Amc,j

12.0  0.8A 18.0  1.5B 17.1  1.2B

0.067  0.003 0.073  0.004 0.053  0.005

14.3  0.7A 27.9  0.7B 40.6  4.8B

194  10A 273  11B 367  24D

72.8  2.4A 91.3  3.6B 77.6  11.4AB

107  6 145  11 123  22

Shenzhen

Saa,j Scb,j Amc,j

10.5  1.4A 13.4  0.8A 19.8  2.1C

0.054  0.005 0.040  0.015 0.051  0.007

10.9  1.6A 12.0  0.2A 26.4  3.3B

202  12A 455  4A 546  33B

30.6  1.1A 44.9  4.8B 106  2C

45.7  5.0A 54.2  6.2A 145  11B

Three species of multivariate analysis-of-variance (MANOVA)k

df Site Species Species  Site

1, 2, 2 3.566 22.277*** 8.067**

1, 2, 2 2.783 8.878** 3.321

1, 2, 2 24.733*** 35.728*** 2.023

1, 2, 2 0.067 26.979*** 6.222**

1, 2, 2 19.098** 27.164*** 26.254***

1, 2, 2 21.553*** 14.410**** 12.680**

a b c d e f g h i j k

Sa, Sonneratia apetala. Sc, Sonneratia caseolaris. Am, Avicennia marina. Amax, maximum assimilation rate. FCO2, apparent quantum efficiency. LCP, light compensation point. LSP, light saturation point according to light–response curves. Vc,max, maximum rate of carboxylation by Rubisco. Jmax, PAR-saturated rate of electron transport according to A–Ci curves. Different capital letters represent significant differences among three species in each study site according to within-site one-way ANOVA followed by LSD test at p < 0.05. Levels of significance are shown as: *p < 0.05, **p < 0.01, ***p < 0.001.

LCP and LSP than those of the introduced Sonneratia apetala. In Shenzhen, the two introduced Sonneratia species had similar Amax, LCP and LSP, but their values were significantly lower than those of the indigenous mangrove species, A. marina (Table 3). There were no significant differences in FCO2 values between the introduced and the indigenous mangrove species in both Hainan and Shenzhen. Although the shapes of A–Ci curves of the introduced and the indigenous mangrove species were similar in Hainan, a significant difference in the relationship of A to Ci between the introduced and native mangrove species was observed in Shenzhen (Fig. 5C,D). The values for Vc,max and Jmax calculated from the A–Ci curves for these mangrove species are shown in Table 3. In Hainan, the values of Vc,max, Jmax were comparable among the three mangrove species. In Shenzhen, however, the introduced species Sonneratia caseolaris and Sonneratia apetala had significantly lower Vc,max and Jmax, than the native species Avicennia marina. 4. Discussion We found that leaf gas exchange of the introduced Sonneratia was not higher than the indigenous mangrove species in both locations (Fig. 2). Our findings on mangrove leaf gas exchanges were inconsistent with previous studies which had shown higher leaf gas exchanged for the invasive species (Durand and Goldstein, 2001; Ewe and Sternberg, 2003). After more than 20 years of cultivation, the earliest introduced Sonneratia apetala seedlings now formed a mono-specific forest with 15 m height in Hainan (Wang et al., 2002). The fast growth of S. apetala in Hainan might due to its similar A, E, gs, WUEi and PNUE to the indigenous mangrove species. Water use efficiency is one of most important traits contributing to growth, survival, and distribution of plant species. The foliar d13C values provided a useful long-term indication of photosynthetic performance and plant metabolism (Farquhar et al., 1989) and water use efficiency during growing season (Ehleringer et al., 1986, 1987; Clough and Sim, 1989; Hue et al., 1994; Lloyd and Farquhar, 1994). Sonneratia apetala had higher d13C value than the native species Aegiceras corniculatum and Kandelia candel in Hainan, suggesting that the introduced species have higher long term water

use efficiency than some of the native mangrove species (Fig. 3, Table 3). The lower leaf N content and higher A contributed to the higher PNUE of the introduced S. apetala than almost all of the indigenous mangrove species except Sonneratia caseolaris in Hainan (Fig. 4, Table 3). There were close relationships among leaf N concentrations, Rubisco concentrations and photosynthetic rates (Makino et al., 1994; Gonzalez-Real and Baile, 2000). Our results indicated that the introduced S. apetala had lower gas exchange rate, nitrogen and water use efficiencies than the native S. caseolaris and Avicennia marina in Hainan. As an indigenous species in Hainan, Sonneratia caseolaris has been introduced to Shenzhen for 15 years. The introduced S. caseolaris grew very fast even exceeded the grow rates of another introduced species Sonneratia apetala in Shenzhen (Wang et al., 2002), which was consistent with our present results of higher A, E and WUEi for S. caseolaris than S. apetala. Photosynthetic nitrogen use efficiency (PNUE) of S. caseolaris in Shenzhen was almost two times higher than that of all the other mangrove species (Fig 4H). In addition, S. caseolaris in Shenzhen had much higher assimilation rate (A) than most native mangrove species except Avicennia marina (Fig. 4A). High PNUE resulted from high photosynthesis at a low level of leaf nitrogen which potentially provided a competitive edge for exotic co-occurring with native species (Ewe and Sternberg, 2003). If the N supply changed during the course of the destruction of mangroves, or on the tidal flat without mangroves, the introduced S. caseolaris in Shenzhen might become a more competitive species than another introduced S. apetala because of its higher PNUE. The two Sonneratia species are evergreen woody mangrove plants used often as the pioneers in mangrove reforestation in the intertidal zones for a long time in China (Wang et al., 2002). A field study by Zan et al. (2003) found that Sonneratia apetala, and Sonneratia caseolaris had significant overlap in their ecological niches according to a field investigation. Also, our results indicated that S. apetala and S. caseolaris overlapped in the patterns of gas exchange of long-term effect, such as PNUE, long-term water use efficiency and leaves N content. A potential competition between two Sonneratia species in similar ecological niches should not be neglected in further research.

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Important photosynthetic patterns showed by light–responses curves of plants including Amax, which reflects the rate of diffusion of CO2 to Rubisco, the activity of Rubisco, and/or the rate of regeneration of RuBP (Farquhar et al., 1980). Contrary to the original hypothesis that the introduced Sonneratia species had better adaptive strategies in photosynthetic capacities than the native mangroves species, the introduced Sonneratia apetala had much lower Amax and LSP than the native Sonneratia caseolaris and Avicennia marina in Hainan, suggesting its lower carbon assimilation capacity than the native mangrove species. FCO2 was the efficiency of light utilization in photosynthesis and reflected the number of moles of CO2 fixed per mole quantum absorbed by leaf (Long et al., 1993). In-significantly differences of FCO2 were found among three species in Hainan (Table 3). Lower LCP was found in the introduced S. apetala, suggesting a better adaptation to low light condition (Krauss and Allen, 2003). A similar tendency occurred in Shenzhen when Sonneratia caseolaris became an introduced species, where the two introduced Sonneratia had lower Amax than the native Avicennia marina (Table 3). Lower photosynthetic performance (Amax, LCP and LSP) of the both introduced Sonneratia in Shenzhen also suggested lower carbon assimilation capacities in the introduced sites. However, lower Amax and LCP of both Sonneratia species than the indigenous A. marina also indicated a better adaptation to low light regime but not being able to respond to more favorable conditions (Krauss and Allen, 2003). Pattison et al. (1998) have suggested that successful invasive species had some physiological traits which increased the light capture. Our results of lower LCP and Amax of the introduced Sonneratia in both study sites indicated that they were well adapted to a low light regime, which along with comparable A (Fig. 2A,B) with the indigenous species suggested ready adaptation to the new habitat. However, more evidence of the environmental resistance of the introduced Sonneratia, such as the LCP of non-native species modified with salinity and tidal flooding, is still needed for the assessment of their invasive potentials. Vc,max and Jmax values obtained from A–Ci curves had similar tendency to those of Amax, LCP and LSP. Vc,max, which was positively correlated with the content and activity of leaf Rubisco, reflected the maximum rate of carboxylation by Rubisco, while Jmax indicated the PAR-saturated rate of electron transport (Farquhar et al., 1980). Previous studies have proved that environmental stresses impressed leaf Vc,max and Jmax, further decreased the carboxylation efficiency of Rubisco enzyme and reduced the rate of electron supply by the electron transport system for RuBP regeneration, and limited the available inorganic phosphorus for Calvin cycle (Niu et al., 2008; Youssef, 2007). Our results indicated that the introduced Sonneratia apetala in Hainan had lower CO2 diffusion rates and RuBP regeneration rates, which decreased the photosynthetic capacities and further reduced the competition with the native mangrove species. These results did not support the hypothesis that introduced Sonneratia had strong adaptive strategies in photosynthetic capacities in the new habitats. The environmental stresses might be other important reasons for different adaptive strategies, which need further research. In addition, lower Vc,max and Jmax values obtained from A–Ci curves were found in both Sonneratia in Shenzhen, which were similar to those in Hainan, indicating lower CO2 diffusion rates and RuBP regeneration rates of the introduced species. 5. Conclusions Our physiological comparisons indicated that the introduced Sonneratia apetala did not have higher gas exchange rate, WUE and PNUE than the native Sonneratia caseolaris and Avicennia marina in Hainan, and both introduced Sonneratia species had similar or

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lower gas exchange rate, WUE and PNUE than the indigenous A. marina in Shenzhen, suggesting little competitive strategies of these introduced Sonneratia species over the native mangrove species in China. The gas exchange rate and WUE of the introduced S. caseolaris in Shenzhen were not significantly higher than the average of the native mangroves species, except for PNUE. The higher PNUE of the introduced S. caseolaris in Shenzhen might contribute to its fast growth rate or even result in a highly competitive pattern which requires further study. In addition, the photosynthetic parameters derived from typical light–response curves and A–Ci curves suggested lower carbon assimilation capacities for the introduced Sonneratia than for the indigenous species in both sites, which also indicated lower competitive advantages of the two introduced species over the native mangrove species in the favorable conditions. Acknowledgements We thank L. Li of the Institute of Botany, CAS, for the analysis of the stable isotopic ratios, Z. Huang in the Administrative Bureau of Dongzhai Harbor Mangroves National Nature Reserve in Haikou, and Y. Wang, Q. Zan and H. Xu in the Administrative Bureau of Neilingding-Futian National Nature Reserve in Shenzhen for their help in the fieldwork. We also appreciate the valuable suggestions from Dr. K.S. Shin and Dr. S.G. Cheung of City University of Hong Kong. This study was partially supported by an NSFC grant to L. Chen (30700092), the ‘‘Bairen project’’ of the Chinese Academy of Sciences to G. Lin, a China Postdoctoral Science Foundation award to L. Chen (20060400529), the Areas of Excellence established under the University Grants Council of the Hong Kong SAR, China (Project No. AoE/P-04/2004) to N. Tam, and a Xiamen University ‘‘Minjiang Scholar’’ program support to G. Lin. References Allen, J.A., 1998. Mangroves as alien species: the case of Hawaii. Global Ecology and Biogeograpaphy Letters 7, 61–71. Allen, J.A., Krauss, K.W., Duke, N.C., Herbst, D.R., Bjo¨rkman, O., Shih, C., 2000. Bruguiera species in Hawaii: systematic considerations and ecological implications. Pacific Science 54, 331–343. Atkinson, C.J., Winner, W.E., 1987. Gas exchange characteristics of Heteromeles arbutifolia during fumigation with sulphur dioxide. New Phytologist 106, 423–436. Baruch, Z., Goldstein, G., 1999. Leaf construction cost, nutrient concentration and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 121, 183–192. Chen, S.P., Bai, Y.F., Zhang, L.X., Han, X.G., 2005. Comparing physiological responses of two dominant grass species to nitrogen addition in Xilin River Basin of China. Environmental and Experimental Botany 53, 65–75. Clough, B.F., Sim, R.G., 1989. Changes in gas exchange characteristics and water use efficiency of mangroves in response to salinity and vapour pressure deficit. Oceologia 79, 38–44. Ding, J., Xie, Y., 1996. The mechanism of biological invasion and the management strategy. In: Peter, J.S., Wand, S., Xie, Y. (Eds.), Conserving China’s Biodiversity (II). China Environmental Science Press, Beijing, pp. 50–55 (in Chinese). Drake, J.A., Mooney, H.A., Di Castri, F., Groves, R.H., Kruger, F.J., Rejmanek, M., Williamson, M., 1989. Biological Invasions: A Global Perspective. John Wiley and Sons, Chichester, 525 pp. Durand, L.Z., Goldstein, G., 2001. Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126, 245–354. Ehleringer, J.R., Field, C.B., Lin, Z., Kuo, C., 1986. Leaf carbon isotope and mineral composition in subtropical plants along an irradiance cline. Oceologia 70, 520–526. Ehleringer, J.R., Lin, Z.F., Field, C.B., Sun, G.C., Kuo, C.Y., 1987. Leaf carbon isotope ratios of plants from a subtropical monsoon forest. Oecologia 72, 109–114. Ewe, S.M.L., Sternberg, L. da S.L., 2003. Seasonal gas exchange characteristics of Schinus terebinthifolius in a native and disturbed upland community in Everglades National Park, Florida. Forest Ecology and Management 179, 27–36. Farquhar, G.D., Caemmerer, S.V., Berry, J.A., 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90. Farquhar, G.D., Ball, M.C., Caemmerer, S.V., Roksandie, Z., 1982. Effect of salinity and humidity on d13C value of halophytes-evidence for diffusional isotope fractionation determined by the ratio of intercellular/atmospheric partial pressure of CO2 under different environmental conditions. Oecologia 58, 121–124.

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