Acta Oecologica 49 (2013) 83e91

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Acta Oecologica
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Original article

Effects of sea level rise on mangrove Avicennia population growth, colonization and establishment: Evidence from a eld survey and greenhouse manipulation experiment
Weizhi Lu a, Luzhen Chen a, *, Wenqing Wang a, Nora Fung-Yee Tam b, Guanghui Lin a, c, **
a

Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen, Fujian 361005, China Department of Biology and Chemistry, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong c Key Laboratory of the Ministry of Education for Earth System Modelling, Center for Earth System Science, Tsinghua University, Beijing 100084, China
b

a r t i c l e i n f o
Article history: Received 24 July 2012 Accepted 12 March 2013 Available online 10 April 2013 Keywords: Accelerated sea level rise Colonization Establishment Growth Mangroves Water use efciency

a b s t r a c t
Mangroves will either face longer tidal inundation or retreat landwards in response to on-going accelerated sea level rise. However, little is known about the growth, regeneration or colonization of mangrove seedlings under the different tidal inundation regimes associated with accelerated sea level rise. In the present study, a eld survey and a greenhouse mesocosm experiment were conducted to evaluate possible effects of accelerated sea level rise on colonization, establishment and seedling growth of a mangrove pioneer species, Avicennia marina. Avicennia populations at different elevations of the intertidal zone on Xiamen Island in Fujian Province, China showed distinctive patterns in both seedling density and plant age. The seedlings at lower elevations had less annual biomass accumulation and population productivity, but higher shoot to root ratios, suggesting that elevation has positive effects on seedling growth. The greenhouse mesocosm experiment with 1-year-old A. marina seedlings utilized ve inundation periods (0, 2, 4, 6 and 12 h in a semidiurnal tidal cycle) and two inundation depths (root immersion and canopy immersion). Both inundation period and depth exerted signicant and negative effects on biomass accumulation, photosynthetic rate, leaf electron transportation and water use efciency. However, the negative effects of canopy immersion were more profound than root immersion. Canopy immersion exacerbated the effects of prolonged inundation, with no seedlings surviving under canopy immersion at the 12-hour treatment. These results suggest that at lower elevations with higher sea level, canopy immersion will have greater negative effects on seedling colonization, establishment and early growth of A. marina. This nding is instrumental in predicting the future dynamics of mangrove forests under increasing sea levels. 2013 Elsevier Masson SAS. All rights reserved.

1. Introduction Mangrove ecosystems are very sensitive to global changes because they are located at the interface between land and sea (Duke et al., 1998; Day et al., 2008). Of all climate change-related effects, sea level rise is the most serious threat to mangroves (Gilman et al., 2008; Chin et al., 2010). Global sea level rise had been

* Corresponding author. Tel.: 86 592 2181430; fax: 86 592 2181430. ** Corresponding author. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen, Fujian 361005, China. Tel.: 86 10 62797230; fax: 86 10 62797230. E-mail addresses: Luzhenchen@xmu.edu.cn (L. Chen), weizhilu@xmu.edu.cn (G. Lin). 1146-609X/$ e see front matter 2013 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.actao.2013.03.009

occurring for more than 20,000 years, however rates of sea level rise appear to be increasing rapidly due to anthropogenic impacts (Erlandson, 2012). Coastal areas of China are especially vulnerable to accelerated sea level rise and associated coastal ooding because of low topography and socioeconomic factors such as highly developed economies and dense populations (Yin et al., 2012). In southeast China, mangroves are also affected by accelerated sea level rise. If sediment surface elevations do not keep pace with sea level rise, mangroves will either retreat landwards or face long periods of tidal inundation (Gilman et al., 2008; Krauss et al., 2008; Abel et al., 2011). If mangroves retreat landwards, there will be increased opportunity for seedling regeneration and colonization (Panapitukkul et al., 1998; Abel et al., 2011). The natural regeneration of a forest plays an important role in community expansion, dispersion and maintenance, as well as in maintaining community

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Fig. 1. (A) Location of eld survey sample plots. E1 to E5 indicate the ve different elevations of the plots: 105, 95, 65, 55, and 45 cm above mean sea level, respectively. (B) Experimental set-up for the greenhouse manipulation experiment showing the tidal tanks used for different immersion treatments. Hollow arrows indicate water owing between tanks B to E, water retreating back to the water container and water reentering the tanks from the water container; h indicates inundation period (hour); RI: root immersion, CI: canopy immersion; and the dotted line indicates water level.

stability and succession (Martinkova et al., 2011). Studies on the regeneration and colonization of mangrove forests at different elevations can provide new insights into how mangrove seedlings respond to tidal inundation and accelerated sea level rise. Previous studies on the potential impact of accelerated sea level rise on mangrove forests focused on growth, physiology, morphology, anatomy and reproduction, and mainly utilized manipulation experiments with water inundation treatments (Ellison and Farnsworth, 1997; Naidoo et al., 1997; Kitaya et al., 2002; Chen et al., 2005; He et al., 2007; Hoppe-Speer et al., 2011). These studies revealed that, with prolonged inundation, mangroves allocated more relative biomass to aboveground structures or grew taller as mechanisms for avoiding tidal inundation. However, these studies focused mainly on the effect of tidal inundation periods (Ellison and Farnsworth, 1993; Buckley et al., 1998; Kitaya et al., 2002; Chen et al., 2005; Krauss et al., 2008). In actuality, water inundation depth as well as inundation period will simultaneously increase with accelerated sea level rise, and these two factors may have different effects on the physiology and growth of different mangrove species due to different distributions in the intertidal zone. Previous research focused either on inundation depth or inundation period, and thus do not provide a complete picture for mangroves in different intertidal zones and with different canopy heights, in terms of their potential sensitivity to accelerated sea level rise. Only a few studies were conducted to investigate mangrove seedling colonization and establishment under accelerated sea level rise scenario (Ye et al., 2004; McKee et al., 2007; Di Nitto et al., 2008; Hickey and Bruce, 2010), and studies of population structure and productivity responses (e. g.

forest density, tree height, biomass increment) were rare. Thus, there remain many knowledge gaps about the growth, regeneration and colonization of mangrove seedlings as sea level rise accelerates in response to global warming. In this study, we investigated the following questions: (1) how do mangrove population structure and productivity change with accelerated sea level rise? (2) Is inundation depth or inundation period correlated to the observed negative effects of tidal inundation on mangrove seedling growth and colonization? We hypothesized that (1) the growth, population structure and productivity would be devastated with the accelerated sea level rise; (2) inundation depth exerts a stronger inuence on seedlings facing accelerated sea level rise. Avicennia marina was selected in this study because it is a widespread mangrove species with a large distribution in South Asia and Australia (Duke, 1991; Lin, 1999). Compared with other mangrove species, A. marina occupy more seaward habitats and exhibit relatively higher waterlogging tolerance, achieving higher survival over a wider tidal range (Ashford and Allaway, 1995; Lin, 1999; He et al., 2007; Xiao et al., 2009). In this study, mangrove growth and biomass were investigated in a eld survey to determine the effects of accelerated sea level rise on population structure and productivity. The separate and interactive effects of inundation period and depth on the growth and leaf physiology of A. marina seedlings were investigated in greenhouse manipulation experiments. The greenhouse investigation focused only on seedlings since they are more likely to be immersed if sea levels meet the projection of rising at least 30 cm over current levels by 2100 (IPCC, 2007; Kemp et al., 2011).

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2. Materials and methods 2.1. Description of study sites The study sites for the population survey were located in an abandoned sh pond, adjacent to a mudat on the northwest coast of Xiamen Island, Fujian Province of China (24 320 N, 118 060 E, Fig.1A). The pond area was greater than 1 ha, and had been undergoing natural succession for more than 10 years. The mangrove forest was dominated by A. marina with most of individuals less than 10 years old. The mean annual temperature in Xiamen was estimated to be 20.7  C and the mean annual rainfall was 1387 mm according to observations of the Xiamen Meteorological Observatory (Chen, 2005). The tidal regime at the site was regular semidiurnal with an average tidal range of 3.96 m, and a high water depth of 5.39 m and low water depth of 1.43 m (Chen, 2005). 2.2. Field survey and sampling The eld sample plots were divided into ve classes according to tidal elevation, where Plot E1 represented the highest elevation, and Plot E5 represented the lowest elevation. For each plot, we measured water depth at tidal ood slack periods, and then calculated elevations according to tidal prediction tables. Elevations were 105, 95, 65, 55, and 45 cm above mean sea level for Plot E1 through E5, respectively. For each elevation plot except E4, four replicate subplots were surveyed (Fig. 1A). Because of the area limitation, Plot E4 had only three replicates. After determining the number of trees in each plot (Plot E1 to E5), all trees within the plots were tagged and the population density was calculated. In addition, tree height, stem base diameter and canopy breadth were also measured. One standard tree in each plot was selected and harvested. The stem, leaves, owers and roots of each sampled tree were separated. We determined the age of each tree roughly according to stem rings. Although some research indicates that A. marina do not have annual rings (Tomlinson, 1995), other sources point out that in subtropical mangroves, stem rings are coincident with annual rings (Yu et al., 2007). In our rough estimate for tree age, we accepted stem ring as the annual ring. Biomass was determined after oven drying for 72 h at 60  C after constant weights were attained. Annual biomass increment (ABI), population productivity (PP) and biomass ratios of shoot to root (S/R) were calculated according to the following equations.

dry weight was used to calculate soil bulk density. Subsamples of soil were air-dried, ground and sieved to a ne power for the determination of total organic carbon (TOC) and soil texture. TOC was determined on acidied samples by standard methods using a Leco induction furnace (Blakemore, 1987). The clay, silt and sand percentage of soil samples were determined using the plummet balance method (Hutton, 1955). 2.4. Seedling preparation for greenhouse manipulation experiment Healthy and mature viviparous propagules of A. marina were collected from Zhangjiang Estuary Mangrove Nature Reserve in Zhangzhou Country, Fujian Province, China (23 550 N,117 240 E). The propagules were grown in a greenhouse at Xiamen University, which had an average daily temperature of 24 8  C and relative humidity of 80 10% during the treatment days. The mid-day photosynthetic active radiation (PAR) was about 700 mmol photons m2 s1, during the sunny treatment days which were measured from 10:00 to 16:00. The propagules were irrigated every two days with articial seawater with a salinity of 15&, similar to the eld mangrove areas salinity of 17&. The articial seawater was prepared by diluting seawater collected from the west coast of Xiamen, with salinity ranging from 22 to 28&, with local tap water. When the seedlings developed the rst two pairs of leaves, and height was 16.4 0.2 cm (mean and standard error, n 20), they were transplanted to pots and placed in the tidal tank system described below. 2.5. Experimental design of greenhouse studies According to our eld observations, water inundation duration in mangrove habitats in Southern China is generally less than 6hour in a tidal cycle. The inundation period during a single tidal cycle varies depending on the elevation of the intertidal area. The four inundation periods for the selected treatments were 0, 2, 4, and 6-hour during a semidiurnal tidal cycle. A 12-hour inundation treatment was also included as the fth inundation period to simulate the scenario that seedlings were inundated throughout an entire semidiurnal tidal cycle, which represented the longest water inundation. Each inundation period treatment had two different water inundation depths e root immersion (RI) and canopy immersion (CI) e to simulate current conditions and future accelerated sea level rise scenarios for mangroves at low and midintertidal zones. All seedlings were inundated twice daily except the 0-hour inundation treatment. To simulate tidal inundation conditions with different inundation depths and periods, a tide tank system using six plastic tanks (65 cm 50 cm 50 cm) was constructed as Fig. 1B, also refer to Chen et al. (2005). Tank A held articial seawater throughout the tidal cycle to simulate the 12-hour inundation. PVC pipes connected Tank B through Tank E. The total time to ll each tank with articial seawater to the predetermined water level was two hours. Tank B, which simulated the 6-hour inundation lled with articial seawater from the water container rst. When Tank B was full, the water overow spilled into Tank C, and so on. When Tank E was full, all of the water in Tanks B, C, D and E discharged back into the water container via timer-controlled pumps. The seawater in the tidal tank system was renewed every two weeks to reduce contamination. To achieve two different inundation depths, seedlings subjected to the RI treatment were elevated by a 30 cm high platform while those subjected to the CI treatment were placed in the bottom of the tank (Fig. 1B). There were 10 pots of seedlings in each tidal tank, with half on the platform (RI) and the other half on the bottom of the tank (CI). For the RI treatment, water submerged the seedling to the junction between the stem and the root, while for

Annual biomass increment ABI

Total Biomass Tree Age

Population productivity PP

Total plant biomass Forest area Tree age

  S Aboveground biomass Shoot=root ratio R Belowground biomass

2.3. Soil measurements In the eld survey, ve soil samples were collected in each plot to measure the soil pH, salinity, bulk density, organic carbon and soil texture. Only one soil sample was measured in Plot E5 because of the high homogeneity revealed in our preliminary experiment. Soil pH and salinity were measured by portable pH/salinity indicator (Thermo Electron Corporation, USA). Bulk density was determined by the volumetric ring method (Blake, 1965). Volumetric ring samples were collected using 90 cm3 sharpened rings at 0e20 cm depth. Samples were oven-dried at 80  C for 72 h and the

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Table 1 Topsoil physical and chemical properties and vegetation structure of A. marina population in the eld plots. Sample group E1 E2 E3 E4 E5 Elevation (cm) 105 95 65 55 45 pH value 6.81 6.96 6.98 7.12 7.06 0.04c 0.01b 0.03b 0.03a Soil salinity (&) 19.42 25.4 31.1 20.5 25.1 1.42c 1.19b 0.36a 1.68c Soil bulk density (g cm3) 1.13 1.17 1.08 1.25 1.22 0.03b 0.02b 0.01b 0.07a Organic carbon content (%) 3.25 3.49 3.44 2.91 2.48 0.09b 0.11b 0.13b 0.05a Soil texture type Silt clay Silt clay Silt clay Clay Silt clay Seedling height (cm) 83.2 91.0 39.7 48.7 30 4.74a 3.73a 3.60b 2.39b Canopy breadth (cm2) 559 498 116 115 41.6 36.8a 67.6a 23.8b 4.42b Vegetation cover (%) 5.59 1.97 1.69 0.24 0.01 0.74a 0.10b 0.25b 0.08c

the CI treatment, the whole seedling, including the canopy was completely submerged (Fig. 1B). Each inundation treatment had three replicates. Each pot, with a dimension of 13-cm height and 12-cm diameter, contained one seedling with two pairs of mature and fully expanded leaves. All seedlings remained in the greenhouse for 100 days. After 100 days of treatment, each seedling in Tanks B, C, D, E and F had four to ve pairs of leaves, however, those under the CI treatment in Tank A were all dead at the end of the experiment. This indicated that they could not stand the 12-hour inundation period combined with canopy immersion. 2.6. Measurements form the greenhouse manipulation experiment 2.6.1. Biomass and growth All seedlings were harvested at the end of the greenhouse manipulation experiments. After separating the leaves, stems and roots, the fresh weight of each part was determined using an electronic balance (Sartorius BS, Goettingen, Germany). The samples were then oven-dried to constant weight at 60  C for 72 h and re-weighed. Seedling height was measured using a ruler. The total leaf area was calculated using the weighing paper cut-outs method (Fisher and Honda, 1977). Specic leaf area (SLA) was dened as leaf area per unit dry weight. 2.6.2. Leaf gas exchange For the greenhouse experiment, photosynthetic rates (Pn) and transpiration rates (Tr) of mature leaves were measured using a portable infrared gas analyzer (LI-6400, Li-cor, Inc., Lincoln, USA) after 76 days treatments (on 17 December, 2008). In order to access the leaves of plants under the CI treatment, water was drained from the tanks until the leaves were above the water. Gas exchange measurements were made on fully expanded leaves, which were conducted between 9:00 am and 11:00 am. The PAR was xed at 1000 mmol m2 s1 by a blue/red light (LI-6400-02 LED light, Li-cor, Inc.) source tted to the leaf chamber and an ambient CO2 concentration was set at 380 2 mmol mol1. Instantaneous water-use efciency (WUEi) was calculated from the ratio of Pn:Tr, and stomatal limitation (Ls) was dened as 1 Ci/C0, with Ci representing intercellular CO2 concentration and C0 for atmospheric CO2 concentration. Three mature leaves for each replicate were chosen for the measurement of Pn and Tr, and the mean values were used for statistical analyses. 2.6.3. Chlorophyll uorescence Chlorophyll uorescence was measured at night for the cultured seedlings with a eld-portable, pulse amplitude, modulated uorometer (PAM-2100, Walz, Effeltrich, Germany). All measurements were taken midway between the base and the tip of mature leaves. Rapid light curves (RLCs) were generated with the PAM-2100 (White and Critchley, 1999; Naidoo et al., 2010). RLCs were plots of electron transport rate (ETR) versus actinic irradiances, applied for 10 s. The PAR was set for the following light levels: 25, 50, 100, 150, 250, 500, 1000 and 1200 mmol m2 s1. The potential maximum electron transport rate (ETRmax), efcient use of light quantum (a) and photoinhibition (b) was calculated using the equation: ETR ETRmax $1

ea$PAR=ETRmax $eb$PAR=ETRmax (modied from Platt et al. (1980)). The half-saturation light intensity (Ik) was calculated by ETRmax/a. 2.7. Statistical analysis Data were examined for normality and homoscedasticity of residual variances. Repeated measures analysis of variance was used to compare eld survey measures of ABI, PP, and S/R ratios change over elevation. For the greenhouse measurements, mean and standard error (SE) values of three replicates were calculated for each of all measured parameters. A parametric two-way analysis of variance (ANOVA) was used to test signicant differences among inundation periods and between inundation depths. If the difference was signicant at p 0.05, a post-hoc test was employed to determine exactly where the difference was. The assumptions of ANOVA, including normal distribution and homogenous variance of the data, were tested. A multivariate ANOVA using the general linear model was used to demonstrate the interactive effects between inundation depth and period on various photosynthetic gas exchange parameters, growth and chlorophyll uorescence. Linear regression analysis was used to evaluate the relationships between Ls and WUEi. The correlation between density and seedling age was also evaluated for the eld investigation. All statistical analyses were performed with SPSS version 13.0 (SPSS Inc., Chicago, USA).

Fig. 2. Changes in seedling density (A) and age (B) of A. marina under different tidal elevation in the eld. A tted curve is shown, where R2 0.53 and 0.88 for seedling density and seedling age respectively, both p < 0.001. E1 to E5 indicate the ve different elevations of the survey plots, which were 105, 95, 65, 55, and 45 cm above mean sea level, respectively.

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Fig. 4. Total biomass (A), specic leaf area (SLA) (B) and shoot root ratio (C) of A. marina seedlings treated with different immersion periods and depths. Mean and standard errors of three replicates are shown. RI: root immersion, CI: canopy immersion. Fig. 3. The annual biomass increment (ABI) (A), population productivity (PP) (B) and shoot to root ratios (S/R) (C) of A. marina seedlings under different tidal elevations in the eld. Different letters above the columns indicate signicant differences in the post-hoc tests.

3. Results 3.1. Field survey 3.1.1. A. marina forest structure and soil parameters In the eld study, tree height increased from Plot E1 to Plot E2 and then declined sharply through E5. The maximum tree height (91 cm) was observed under the Plot E2 elevation. Canopy breadth and vegetation cover signicantly declined with decreased elevation (p < 0.001, Table 1). ANOVA results for mean forest height, canopy breadth and vegetation cover indicated signicant elevation effects on trees and canopy structure (p < 0.001, Table 1). Because of tree density effects, vegetation cover decreased sharply from Plot E2 to E5, while canopy breadth decreased sharply from Plot E3 to E5. Soil pH, salinity and SOC content at different elevations exhibited signicant differences (p < 0.05), but the soil bulk density was not signicantly different (p 0.257) (Table 1). Soil texture was similar across sites except at Plot E3 (Table 1).

3.1.2. Field seedling ABI, PP, and S/R ratios A. marina population density and tree age were linearly related with gradient elevation (both p < 0.001) (Fig. 2A and B). Trees were oldest and had the highest density in the highest elevation plots (E1), while younger and more sparsely distributed trees were observed in the lower elevation plots (e. g. Plot E4 and E5). With increased elevation, the ABI of A. marina trees increased from Plot E1 to Plot E2, and then declined sharply thereafter (p < 0.001). ABI increased from Plot E1 to Plot E2, and then declined thereafter, with the maximum ABI occurring in Plot E2 (Fig. 3A). However, PP decreased from Plot E1 to Plot E4, indicating that lower elevation resulted in lower PP values (p < 0.05) (Fig. 3B). The tree S/R ratios ranged from 2 to 5, and was negatively correlated with elevation (p < 0.001) (Fig. 3C). 3.2. Greenhouse manipulation experiment 3.2.1. Biomass and growth A. marina seedling biomass and SLA showed distinct responses to inundation period in both inundation depth treatments (Fig. 4A and B). The CI-treated seedlings had signicantly lower biomass than those of the RI-treated seedlings in the 2-, 4- and 6-hour

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Table 2 Results of two-way ANOVA tests showing the effects of immersion level and period on total biomass, height, specic leaf area (SLA), net photosynthetic rate (Pn), transpiration (Tr), instantaneous water use efciency (WUEi), stomatal limitation (Ls), d13C, maximum relative electron transport rate (ETRmax), the curves initial slope of rapid light curves (a), photo-inhibition parameter (b) and half-saturation light intensity (Ik) of A. marina seedlings. *, ** and *** indicate signicant differences are found at p 0.05, 0.01 and 0.001, respectively. Parameters Immersion level (L) df Biomass SLA Pn Tr WUEi Ls ETRmax 1 1 1 1 1 1 1 1 1 1 F 38.6** 57.0*** 33.1*** 23.7*** 0.521 5.82* 14.1*** 3.87 5.28* 14.4*** Immersion period (P) df 4 4 4 4 4 4 4 4 4 4 F 0.818 5.32** 9.04*** 6.73** 0.217 0.354 0.872 3.72* 0.360 0.443 Interaction (L P) df 3 3 3 3 3 3 4 4 4 4 F 5.05** 2.62 4.66* 5.39** 0.510 0.785 1.25 2.41 0.729 1.53

a b

Ik

Fig. 6. Relationship between instrinsic water use efciency (WUEi) and stomatal limitation (Ls) under two different water immersion depths. A tted curve is shown, where R2 0.79 and 0.58 for the root immersion (RI) and canopy immersion (CI) respectively, both p < 0.01.

inundation treatments. In the CI-treated seedlings, biomass declined progressively with increasing inundation periods. In the RI-treated seedlings, there was no difference in total biomass among the ve inundation periods (Table 2). The seedling shoot to root ratio did not show any signicant response to inundation period or inundation depth (Fig. 4C; Table 2). However, the CItreated seedlings had signicantly higher specic leaf area (SLA) than those under the RI treatments (Fig. 4C; Table 2). Although SLA showed signicant response to either inundation period or inundation depth, there was no interactive effect of inundation period and inundation depth on this parameter (Table 2). 3.2.2. Leaf gas exchange The net photosynthetic rate (Pn) for the mature leaves in the CItreated seedlings increased from the 0e4-hour treatments, and then

declined thereafter, with the maximum Pn for the seedlings under the 4-hour inundation treatment (Fig. 5B). For the RI-treated seedlings, Pn declined progressively with increasing inundation period, and the maximum Pn occurred in the 0- and 2-hour inundation treatments (Fig. 5B). Transpiration rate (Tr) followed the same trend as Pn (Fig. 5C). Both of these parameters showed signicant interactive effects for inundation depth and period (Fig. 5C; Table 1). Compared to the RI-treated seedlings, the CI-treated seedlings tended to have higher and more variable WUEi (Fig. 6). For both inundation depths, signicant relationships were found between Ls and WUEi (both p < 0.01). However, the slopes were signicantly different between the two inundation depths, with a steeper slope for the CI treatments, indicating the CI-treated seedlings had a larger response in WUEi as Ls increased. 3.2.3. Chlorophyll uorescence The ETRmax in the CI-treated seedlings was lower than that in the RI-treatment (Table 3). For the CI-treated seedlings, the ETRmax declined from the 0- to 12-hour inundation treatments, indicating that longer inundation periods resulted in lower ETRmax values (p 0.045). For the RI-treated seedlings, inundation period did not have a signicant effect on ETRmax (p > 0.05) (Table 3). Quantum use efciency (a) was signicantly affected by inundation period, but photo-inhibition (b) and half-saturation light intensity (Ik) were affected only by inundation depth (Table 3). There were no significant interactive effects of inundation depth and period on these uorescence parameters. 4. Discussion 4.1. Effects of sea level on mangrove colonization Our eld survey results supported the hypothesis that accelerated sea level rise will have strong negative impacts on forest growth, colonization and establishment. The population density and tree growth of A. marina were negatively correlated with tidal elevation. Previous studies pointed out that sufcient available propagules and fruit dispersal ranges inuence the initial stage of colonization (Clarke and Allaway, 1993; Blanchard and Prado, 1995; Kamali and Hashim, 2011). Kumara et al. (2010) also showed that high seedling density benets the speed of sedimentation, which also benets mangrove colonization and establishment. For mangrove populations, zonation patterns typically coincide with gradients in physico-chemical factors, such as tidal inundation, soil redox potential, salinity, pH, and sediment nutrients

Fig. 5. Assimilation rate Pn (A) and transpiration rate Trmmol (B) of mature leaves of A. marina seedlings under different immersion periods and depths. Mean and standard errors of three replicates are shown. RI: root immersion, CI: canopy immersion.

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Table 3 Results of relative electron transport rate curve regression by ETR ETRmax $1 ea$PAR=ETRmax $eb$PAR=ETRmax for A. marina seedlings under different inundation periods and depths (RI: root immersion; CI: Canopy immersion). Parameter ETRmax RI CI RI CI RI CI RI CI 0h 57.1 52.6 0.33 0.32 0.00 0.01 174 167 8.89 1.92 0.01 0.00 0.01 0.00 23.8 7.88 2h 58.0 50.0 0.33 0.37 0.00 0.01 179 137 5.35 2.15 0.01 0.01 0.00 0.00 17.9 8.00 4h 62.7 47.0 0.33 0.35 0.01 0.01 194 135 8.85 1.79 0.02 0.01 0.01 0.00 35.7 7.35 6h 61.3 43.7 0.34 0.35 0.00 0.01 184 126 3.10 2.61 0.01 0.01 0.00 0.00 16.8 6.66 12 h 50.3 47.3 0.32 0.32 0.00 0.01 158 150 1.84 3.72 0.01 0.01 0.00 0.00 8.21 12.3

a b
Ik

ETRmax: maximum relative electron transport rate; a: the curves initial slope of rapid light curves; b: photo-inhibition parameter; Ik: half-saturation light intensity.

(McKee, 1995). Inundation depth and duration depend on seedling position in the tidal zones (Ye et al., 2003; Krauss et al., 2008; Ye et al., 2010). Present research suggested that the soil environment including pH, salinity and SOC content at high elevation was in favor of the seedling colonization and growth. Our results suggest that different elevations in the tidal zones result in different forest structure patterns, even though there were sufcient propagules in all plots. As shown in Fig. 2, seedlings density and average age gradually increased with increasing elevation, implying that higher elevation benets to seedling colonization and growth. As sea level rise accelerates, the elevation of mangroves may descend to a lower level (e.g. the elevation of Plot E1 will shift to that of Plot E3), which would severely affect the mangrove community at the lower elevation (Plot E5), as seedlings would die as a result of serious waterlogged stress (Ross et al., 2000; Sanders et al., 2008; Rivera-Monroy et al., 2011). At the same time, some propagules in lower plots will dispersed to higher elevation with shorter tidal immersion periods (e.g. the shift from Plot E4 to Plot E2). However, dams and levees built landward of many mangrove forests would prevent the retreat of mangrove forests (Fan and Li, 1997; Colonnello and Medina, 1998). This provides further evidence that accelerated sea level rise would limit seedlings colonization, establishment, and growth of mangroves. 4.2. Impact of canopy immersion and prolonged inundation on mangrove seedling growth The present study also demonstrated that, when compared with prolonged inundation, canopy immersion exerted greater negative impacts on biomass accumulation and almost all of the leaf physiological parameters measured for the A. marina seedlings. This supports the hypothesis that complete canopy immersion by seawater will have greater negative effects on the growth and leaf physiology of mangrove seedlings than will prolonged inundation. If inundation occurs only in the root systems, A. marina seedlings survived and maintained a reasonable growth, even in non-stop inundation (i.e. the 12-hour inundation in a semi-diurnal tidal cycle). However, when the canopy was immersed for 2 h or longer, seedlings of the same species either could not survive the 12-hour inundation treatment (after 10 weeks) or maintained signicantly lower growth. Ashford and Allaway (1995) reported that the inner parts of A. marina seedlings contain many gas spaces connected to each other that form a continuous exchange with the atmosphere. When the roots are immersed, the gas space continuum will have access to the atmosphere through the stomata, and leaves can serve as a source of photosynthetically-produced oxygen for the seedlings (Laan and Blom, 1990). However, in complete canopy immersion, the gas exchange is blocked which seriously inhibits photosynthetic assimilation and respiration. Our results indicated that A. marina seedlings could maintain normal or increased growth and physiological processes under the

2- through 6-hour tidal inundation periods. This suggested that, as a pioneer species, A. marina adapts well to changing inter-tidal habitats and develops tolerance to various tidal inundations. He et al. (2007) also reported that A. marina seedlings on the lower water tidal ats grew quicker in terms of height, diameter, leaf production and biomass. They also accumulated more neonatal biomass than those on the mean water mudats. Similar results were found for other mangrove species, such as Rhizophora mangle, Kandelia obovata and Bruguiera gymnorrhiza (Ellison and Farnsworth, 1993, 1997; McKee, 1996; Kitaya et al., 2002; Ye et al., 2003, 2004; Chen et al., 2004; Cardona-Olarte et al., 2006). These results indicated that the duration of inundation affected the growth and development of mangrove seedlings. Hovenden et al. (1995) demonstrated that, in younger mangrove plants, there was sufcient aerenchyma to supply the oxygen requirements of the root system for a period of about 1.5e3.5 h per tide. When the inundation periods exceed this time, the plants become anaerobic and consume more energy in order to maintain their metabolisms. The A. marina seedling biomass accumulation, as well as many foliar photosynthetic properties such as net photosynthetic rate, transpiration rate and stomatal conductance showed signicant interactive effects between inundation period and depth. This suggested that future accelerated sea level rise is likely to reduce the photosynthesis and growth of A. marina seedlings due to the synergistic effects of tidal inundation period and depth. Such impacts were less profound than, or different from, previous studies when only either inundation period or inundation depth was considered. In the present study, there were no signicant differences in seedling growth among different inundation periods; however, there were signicant differences between the two inundation depths.

Fig. 7. Correlation between plant productivity and tidal elevation for A. marina seedlings in the greenhouse manipulation experiment and in the eld. Note that manipulation elevations were inferred according to their respective immersion periods. Numbers above the curve represent the immersion period in a tidal cycle for seedlings in the greenhouse experiment.

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4.3. Effects of accelerated sea level rise on mangrove productivity Both the eld survey and manipulation experiment demonstrated that mangrove productivity was sensitive to predicted aspects of accelerated sea level rise. We found that the tidal elevation in the eld ranged from 45 to 110 cm, corresponding to 4e6 h of tidal immersion in the greenhouse. A linear relationship between plant productivity and tidal elevation was found in the greenhouse experiment (Fig. 7). For both inundation depth treatments (RI and CI), there was an opposite tendency in this relationship (see part 4.2). However, we found that productivity increased with elevation, and then decreased when the elevation exceeded some degree in the eld survey (Fig. 7). With increasing elevation, the range of variation in productivity in the eld was larger than in the manipulated experiment. This was attributed to nutrient (mainly nitrogen) limitation. Generally, mangroves are considered to be limited by nitrogen (McKee et al., 2002; Lovelock et al., 2006). For the seawater used in our manipulation experiment, the inorganic nitrogen (IN) concentration was 54.2 mmol/L (unpublished data), and the total IN input during the 100-day culture period for seedlings was 3.04 g m2. In the eld survey, the soil IN pool was 3.22 g m2 (to the depth of 1 m, unpublished data). Considering tidal water IN input, in the total IN input in the eld was about twice that of the in manipulation experiment. This may be the reason why eld seedlings have higher growth rates at comparable elevations than greenhouse growth seedlings. Thus, nutrient inputs should be considered in further research. We also found it interesting that the suitable range of mangrove elevation in the eld was very narrow when compared to the manipulation experiment results. At elevations lower than 45 cm in the eld, low seedling productivity implied extreme conditions of future accelerated sea level rise, as seen in the most extreme manipulated condition. However, there were few A. marina seedlings distributed at elevation higher than 110 cm at our eld site. Therefore, the future researches on mangrove and sea level change should integrate the immersion period with the tidal regime together. 5. Conclusions The present study indicated that the colonization and establishment of A. marina would be seriously affected by accelerated sea level rise. We concluded that the growth and physiological characteristics of A. marina seedlings were determined by the interactive effects of inundation depth and inundation period, and that inundation depth was a more important limiting factor than inundation period. As predicted by IPCC (2007), global sea level may rise by at least 30 cm by 2100, and A. marina seedlings may suffer negative impacts from accelerated sea level rise in the near future. Accelerated sea level rise will occur gradually but there is little information so far regarding the possible acclimation potential of mangroves to gradual changes in sea levels. In order to better predict the dynamics of mangrove communities, future studies are needed to provide more specic information on the responses of mangroves to accelerated sea level rises, especially focusing on the increase in inundation depths. Acknowledgments The authors would like to thank Yihui Zhang, Jin Wang, Hui Chen, Jiemin Guo, Canmou Wang, Xia Yuan and Ronghao Peng for their assistances and advice throughout the various stages of the study. We thank Abby Lunstrum, Julie Doumbia and Yvonne M. Jeary for improving English language. This research was supported nancially, in part, by grants from the Chinese National Science

Foundation (30930017 and 30700092) and the National Basic Research Program of China (2009CB426306).

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