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Propagule types and environmental stresses matter in saltmarsh plant restoration
Ecological Engineering 143 (2020) 105693
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Propagule types and environmental stresses matter in saltmarsh plant restoration Qun Zhanga,b, Shiyun Qiua, Yi Zhua,b, Xinhong Cuib, Qiang Hea, Bo Lia,
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a
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, and Institute of Eco-Chongming (IEC), Fudan University, Shanghai 200438, People’s Republic of China b Shanghai Academy of Landscape Architecture Science and Planning, and Shanghai Engineering Research Center of Landscaping on Challenging Urban Sites, NO. 899 Longwu Road, Shanghai 200232, People’s Republic of China
A R T I C LE I N FO
A B S T R A C T
Keywords: Scirpus mariqueter Degraded wetlands Environmental niche Propagules Corm shoots Seedlings Plantlets Population restoration Genetic diversity Synergistic effects
Restoration of degraded saltmarshes has attracted global attention, which makes disentangling the factors that determine target species success critically important. The pioneer plant Scirpus mariqueter in the Yangtze River estuary saltmarshes is rapidly declining due to plant invasion. It needs to be protected and restored, but the effects of environmental factors and propagule types on its restoration success are unclear. We examined the environmental niche of three propagule types (seedlings, corm shoots and plantlets) of Scirpus mariqueter under water level, salinity and nitrogen treatments in a greenhouse experiment. We found that water level was the most critical environmental factor limiting plant performance, followed by salinity. Nitrogen addition inhibited propagule growth in intermediate water level and salinity treatments. There were significant three-way interactions between water level, salinity, and nitrogen addition: Scirpus mariqueter performed best in treatments of low salinity + low to intermediate water levels + high nitrogen. Corm shoots outperformed plantlets and seedlings. Our results suggest that planting corm shoots under intermediate salinity and high water level conditions will enhance the restoration success of Scirpus mariqueter in the saltmarshes of the Yangtze River Estuary.
1. Introduction Saltmarshes are one of the highest valued ecosystems in terms of service provision per unit area (Costanza et al., 1997). They provide valuable services to humans, including the production of materials and food, coastal protection, water purification, carbon sequestration, and education (Barbier et al., 2011; Möller et al., 2014). Nonetheless, human activities such as introduction of invasive plants have led to degradation of these coastal ecosystems globally (Zedler and Kercher, 2005; Bayraktarov et al., 2016). Half of global saltmarshes have been destroyed over the past 50 years, with loss continuing at a rate of 2% each year (Lotze et al., 2006; da Silva Copertino, 2011). Recognition of the potential impact of saltmarsh loss among academics and governmental agencies has led to growing interest in saltmarsh restoration to enhance ecosystem persistence and functioning (Broome et al., 1988; Cronk and Fennessy, 2016). Saltmarsh restoration is complex since restoration goals and targets vary from place to place and degradation involves a range of changes in species abundance and ecosystem functioning (Zedler, 2000). Consequently, saltmarsh restoration presents uncertainties and challenges.
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In practice, vegetation restoration can typically be improved by fertilization, hydrological control and species selection. However, few studies have examined the role of propagule types in restoration success (Seliskar, 1995; Mauchamp et al., 2002; Zhou et al., 2003; Jones et al., 2016). In addition, how differential responses of propagule types to environmental factors impact restoration success is unclear. The availability of viable propagules of target species may also be important (Broome et al., 1988; Mossman et al., 2012). Acquisition of propagules from the wild for restoration may damage to natural populations. Thus, it is important to explore propagule options when restoration target species are limited in large revegetation projects. Tissue culture is an important technique to rapidly obtain plantlet propagules. Whether plantlets perform as effectively as other types of propagules in restorations, however, is unclear. The growth and zonation of saltmarsh plants is related to abiotic factors, including salinity (Chambers et al., 1998; Huckle et al., 2000; Naidoo and Kift, 2006), tidal inundation (Person and Ruess, 2003; Ennis et al., 2014), and nutrient levels (Lohrer and Wetz, 2003; Neves et al., 2010). High soil salinity can prevent seed germination, whereas low soil salinity can promote succession of halophytes to glycophytes
Corresponding author at: Institute of Biodiversity Science, Fudan University, 2005 Songhu Road, Shanghai 200438, People’s Republic of China. E-mail address: [email protected] (B. Li).
https://doi.org/10.1016/j.ecoleng.2019.105693 Received 30 August 2019; Received in revised form 20 November 2019; Accepted 21 November 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.
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culture dishes in early April 2013 to obtain corm shoots and seedlings. The dishes were placed in a plastic greenhouse with sunlight exposure, at 15–25 °C. Plantlets were obtained from tissue culturing, and the mature seeds of Scirpus mariqueter were used as explants. The procedures of tissue culture contained germ-free germination, induction of multiple shoots, multiplication, rooting and transplanting (Zhang et al., 2016). The common greenhouse experiment was conducted at the Hydrophyte Germplasm Resource Garden in the Shanghai Academy of Landscape Architecture Science and Planning (31° 9′15.7″ N, 121° 26′36.8″ E). The greenhouse was covered with transparent plastic to exclude rainwater, had 45 experimental cement pools and temperature were close to the ambient outdoor conditions.
(Wolters et al., 2005). Inundation can suppress the colonization of some saltmarsh species (Tolley and Christian, 1999), and inundation frequency can affect the dominance of saltmarsh plants (Bockelmann et al., 2002). Increased coastal nitrogen deposition may lead to saltmarsh loss, which reduces ecosystem services provided by saltmarshes (Bertness et al., 2008; Deegan et al., 2012). It is crucial to investigate these effects to maximize salt marsh restoration success. Saltmarshes on Chongming Island in the Yangtze River estuary, Shanghai, China, are important coastal ecosystems (Li et al., 2009). A native species, Scirpus mariqueter, dominates undisturbed saltmarshes as a key species and an ecosystem engineer (Chen et al., 2004). From 2003 to 2014, however, its abundance in Shanghai dropped from 7602 hm2 to less than 550 hm2 largely due to Spartina invasions (Shanghai Chongming Dongtan National Reservec, 2015), and is now threatened with local extinction. The loss of Scirpus mariqueter populations can affect the integrity, ecosystem services, and health of the Yangtze River Estuary (Li et al., 2009). For example, loss of Scirpus mariqueter has reduced various taxa of native biodiversity (Li et al., 2009), especially birds (Gan et al., 2009). Therefore, protection and restoration of this species is needed. To curb further expansion of Spartina alterniflora and restore shorebird habitats, the local government launched a project in 2012 to control Spartina invasion and restore shorebird habitats at Chongming Dongtan. The goals of the project included removal of Spartina, improvement of shorebird habitats and restoration of native plant populations. Presently, the majority of the Spartina alterniflora had been removed to encourage recovery of Scirpus mariqueter (Tang, 2016). However, how different Scirpus mariqueter propagule types respond to environmental factors (i.e. salinity, inundation and nutrient levels) that can inform of restoration success are unclear. This poses the question: how should propagules be selected to maximize population recovery and restoration success? We conducted a greenhouse experiment to examine the environmental niches of three types of propagules of Scirpus mariqueter in different water level, salinity, and nitrogen treatments. Specifically, we addressed the following questions: (1) How do salinity, water level, and nitrogen availability affect the performance of Scirpus mariqueter? and (2) Do the effects of environment factors differ among Scirpus mariqueter propagule types?
2.3. Experimental design Three types of propagules (PR; corm shoots (CS), seedlings (SE), and plantlets (PL)) of similar size (about 10 cm length of each propagule) were selected as experimental materials for the common garden experiment. To make the initial size of the three propagule types as similar as possible, we germinated the seedlings two weeks earlier than corm shoots and plantlets because seedlings grow slower after germination than the others. A fully factorial experimental design was used (Zuur et al., 2009; Harrison et al., 2018), manipulating propagule type and three environmental factors, water level (WL), salinity (SA), and nitrogen addition (NA). Each environmental factor had three levels (−20, 0 and 20 cm to the substrate surface for water level; 2, 10 and 18 g/kg for salinity; 0, 20 and 40 g·m−2·y−1 for nitrogen addition). Water level was referenced to the elevation range in the restoration area and previous experience (Wang et al., 2010); salinity was referenced to the measured value range of water salinity in the restoration area between 2010 and 2012 (1.8–17.8 g/kg) and range of fluctuation of annual mean salinity in natural habitats (Yin et al., 2018); nitrogen addition simulated typical seawater inorganic nitrogen input, the high condition was about 1.6 times of that in Adam Langley et al. (2013), and the range was set according to the results of preliminary experiments. Each treatment combination was replicated four times, resulting in 324 pots (three water levels × three salinity levels × three nitrogen addition levels × three propagules × four replicates). On May 10, 2014, we planted all the propagules in pots (20 cm diameter and 18 cm height) filled with soil collected from the restoration area. In order to ensure one healthy plant per pot, we planted 20 seedlings or 10 corm shoots or 10 plantlets per each pot at beginning, which were then thinned to one focal plant per pot one month after transplantation. We replaced plants that died with new ones during the first two weeks after transplanting. Pots were placed in the 36 cement ponds (100 cm long, 100 cm wide, and 50 cm height with eight small holes in the bottom) with different levels of salinity and nitrogen addition (Appendix Table A1). We placed nine pots (three pots for each of the three types of propagules) into each cement pool. The pools were randomly assigned to one of the three water levels; pots were placed at different heights to achieve different water levels, i.e., −20, 0, and 20 cm. Water was supplied regularly to maintain water level due to evaporation, and salinity was adjusted twice per month. A concentrated nitrogen solution containing equal proportions of ammonium chloride (NH4Cl) and sodium nitrate (NaNO3) was added to the pools fortnightly during the growing season (Ali et al., 2001; Tyler et al., 2007; Ket et al., 2011; Adam Langley et al., 2013). All plants were harvested at the end of September 2014. We counted the ramet number of individuals and the seed number produced per pot. Shoots were cut at the soil surface, and dried at 60–65 °C for three days, while the belowground parts were washed out of the soil using mesh sieves and dried at 60–65 °C for three days. For those pots where all plants died, we set density, seed number, and total biomass as zero.
2. Materials and methods 2.1. Study area The Yangtze estuary is a meso-tidal estuary with semidiurnal tides, and has several alluvial islands, including Hengsha, Changxing and Chongming Islands (Li et al., 2009). Chongming is the oldest and largest of these islands and is the third largest island in China. Geomorphologically, the Yangtze Estuary has a complex structure and provides abundant ecosystem services for human beings and wildlife (Li et al., 2009). Reclamation activities and biological invasion, however, have led to a sharp decline of saltmarshes from 1950s in the estuary (Gu et al., 2018). To prevent range expansion of invasive Spartina alterniflora and restore original habitats, the local government launched a project using integrated methods for invasive plant control and rejuvenation of Scirpus mariqueter and other native species. The project is located in the Chongming Dongtan Bird National Nature Reserve (31°25′~31°38′ N, 121°50′~122°05′ E), on eastern Chongming Island in the Yangtze Estuary (Tang, 2016). 2.2. Propagule materials Corms and seeds of Scirpus mariqueter were collected from ten locations 100 m apart in pure stands of Scirpus mariqueter in the intertidal zone of Chongming Dongtan in the winter of 2012, and stored at 4 °C. Corms or seeds from different locations were mixed and sowed in 2
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Due to the non-normal distribution of data, generalized linear mixed models (GLMMs) were used for examining the effects of water level, salinity, nitrogen addition, and propagule type on plant performance. We used total biomass, density (ramet number per pot), and seed number as response variables. Water level, salinity, nitrogen addition, and propagules were treated as the fixed effects, and ‘pool number’ as a random effect. The GLMMs were analyzed using gamma distribution with the inverse link for total biomass, and the data were (x + 0.001)-transformed (He et al., 2015) to avoid zero values. The effects were tested using likelihood ratio tests (LRT) and the drop1 function in R (Zuur et al., 2009) for GLMMs. Post hoc tests of significant interactions were conducted using the lsmeans function in R (Lenth, 2015; Benítez-Malvido et al., 2018). Where an additive model would explain the data, the significant interactive effects can effectively summarize the main effects in an interpretable way (Lenth, 2012). Furthermore, the results may be misleading due to involvement in interactions. So only the effects of the interaction are presented. The data on density and seed number were analyzed using a Poisson distribution with log link GLMMs, using the GLMMTMB package (Magnusson et al., 2017). For density, the model with four-way interactions did not converge; we therefore included only two- and threeway interactions in the model. For seed number, the models with interactions did not converge, we therefore included only main effects in the model. The significance of effects was tested similarly using the 1 function in R for GLMMs. Post hoc tests of significant interactions were conducted as described above. All analyses were performed with R 3.5.1 (R Development Core Team, 2018).
addition (P < 0.0001, LRT = 57.71; Fig. 1A; Appendix A, Table A2). In the intermediate water level treatment, the total biomass in the intermediate salinity treatment was significantly lower than that in the low salinity treatment only in the high nitrogen addition treatment (post hoc analysis; Appendix A, Table A3; nitrogen addition = 40 g, water level = 0 cm: P2–10 (SA) = 0.004). In the low water level treatment, the total biomass in the intermediate salinity treatment was also significantly lower than the low salinity treatment in the low nitrogen addition treatment (post hoc analysis; Appendix A, Table A3; nitrogen addition = 0 g, water level = −20 cm: P2–10 (SA) = 0.031). However, salinity did not affect the total biomass at low or high water levels, nor in low or intermediate nitrogen addition treatments (P > 0.05 in all cases). In all nitrogen addition × water level treatments, total biomass in the high salinity treatment was significantly lower than in low or intermediate salinity treatments (P < 0.05 in all cases; salinity = 18 g/ kg, total biomass = 0 g), except under the low nitrogen addition and low water level conditions (nitrogen addition = 0 g, water level = −20 cm: P10–18 (SA) = 0.055). Total biomass was also significantly affected by the interaction between water level and propagule type (P < 0.0001, LRT = 379.43; Fig. 1(B); Appendix A, Table A2). In the low water level treatment, the biomass of plants grown from corm shoots was significantly higher than those from seedlings (post hoc analysis; Appendix A, Table A3; water level = −20 cm: PCS-SE(PR) = 0.024). In the intermediate water level treatment, the biomass of plants grown from seedlings was significantly lower than those from both corm shoots and plantlets (water level = 0 cm: PCS-SE(PR) = 0.010, PSE-PL(PR) = 0.018), while in the high water level treatment, total biomass of plants grown from corm shoots was significantly higher than those from both seedlings and plantlets (water level = 20 cm: PCS-SE(PR) < 0.0001, PCS-PL(PR) < 0.0001).
3. Results
3.2. Effects of environmental factors on asexual propagation
3.1. Effects of environmental factors on growth
The density of Scirpus mariqueter decreased as salinity or water level increased (Fig. 2A). Density was also significantly affected by a threeway interaction among salinity, water level, and nitrogen addition (P = .016, LRT = 18.76; Fig. 2A; Appendix A, Table A4). When treated with high nitrogen addition and intermediate water levels, plants under
2.4. Data analysis
The total biomass of Scirpus mariqueter decreased as salinity and water level increased (Fig. 1A), and was also significantly affected by a three-way interaction among salinity, water level, and nitrogen
Fig. 1. A) Total biomass of Scirpus mariqueter in different combinations of water level (−20, 0 and 20 cm), nitrogen addition (0, 20 and 40 g) and salinity (2, 10 and 18 g/kg) treatments. Data shown are means ± SE (n = 12 pots). Different lowercase letters indicate significant differences among three different salinities within the same water level + nitrogen addition treatment combinations. B) Total biomass of three types of propagules in different water level (−20, 0 and 20 cm) treatments. Data shown are means ± SE (n = 36 pots). Different lowercase letters express significant differences among the three types of propagules within the same water level treatment. Test statistics are given in Appendix A: Table A2, A3. Bars without letters illustrate non-significant differences. 3
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Fig. 2. A) Density of Scirpus mariqueter in different combinations of salinity (2, 10 and 18 g/kg), water level (−20, 0 and 20 cm) and nitrogen addition (0, 20 and 40 g) treatments. Data shown are means ± SE (n = 12 pots). Different lowercase letters mean significant differences among three different salinities at the same water level and the same nitrogen addition treatment. B) The density of three types of propagules in different water level (−20, 0 and 20 cm) treatments. Data shown are means ± SE (n = 36 pots). Different lowercase letters show significant differences among the three types of propagules in the same water level treatment. Test statistics are given in Appendix A: Table A4, A5. The bars without letters represent non-significant differences.
informing successful salt marsh restoration.
low salinity treatments exhibited significantly higher densities than plants under intermediate salinity treatments (post hoc analysis; Appendix A, Table A5; nitrogen addition = 40 g, water level = 0 cm: P2–10 (SA) = 0.0001). However, in other nitrogen addition × water level treatments, plants exhibited similar densities at both low and intermediate salinities (P > 0.05 in all cases). Moreover, density was significantly affected by an interaction between water level and propagule type (P < 0.0001, LRT = 201.35; Fig. 2B; Appendix A, Table A4). The pattern of interaction effects on density was similar to that on biomass, and density of plants grown from plantlets was significantly higher than that from seedlings, except in low water level treatments (post hoc analysis; Appendix A, Table A5; water level = −20 cm: PSE - PL (PR) = 0.0005).
4.1. Synergistic effects of environmental factors on plant performance Our study showed that the interaction between high salinity and high water level treatments severely affected the performance of Scirpus mariqueter. All three types of propagules were unable to survive the highest water level and salinity treatments (Figs. 1A, 2A). This is consistent with the results of earlier common garden studies (Huckle et al., 2000; Wang et al., 2010). Previous studies have shown that flooding under saline conditions increased Na+ and Cl− concentrations in shoots, due to increased rates of ion transport (Barrett-Lennard, 2003). These increased concentrations negatively impact plant growth (Barrett-Lennard, 2003). We found that nitrogen addition enhanced the negative effects of salinity on plant performance, but other studies have demonstrated that nitrogen addition can alleviate salinity stress. Our results showed that Scirpus mariqueter performance was significantly affected by an interaction among salinity, water level, and nitrogen addition, and effects on density were broadly similar to those on biomass. In the high nitrogen addition treatment, the intermediate salinity treatment significantly inhibited plant performance, compared with the low salinity treatment, perhaps due to high osmotic pressure in the roots at intermediate salinity levels. Application of nitrate and ammonium increased osmotic pressure of the root system, especially in water-saturated environments, and may promote ion migration (Hessini et al., 2019). Plants experiencing salt stress over the course of several days were highly restricted in their assimilation of nitrate from the nutrient solution, leading these plants to have lower nitrate accumulation in their stems and leaves (Silveira et al., 2001). The salt-osmotic effects evoked by NaCl can damage the root membrane (Maurel et al., 2008), reduce nitrate uptake, restrict nitrates from entering the root xylem (Baki et al., 2000), and reduce the water absorption of plants (Silveira et al., 2001). Such synergistic effects have also been found to occur between grazing and drought, and between salinity and temperature. In drought years, saltmarshes cover was sharp declined with impacts of grazing than in non-drought years (He et al., 2017). Shore molluscs embryonic mortality was significantly higher in response to high salinity in high
3.3. Effects of environmental factors on sexual propagation The number of seeds produced per pot was significantly affected by water level, salinity, nitrogen addition, and propagule type (P < 0.05 in all cases, LRTWL = 49.60, LRTNA = 6.61, LRTPR = 357.71, LRTSA = 40.57; Fig. 3; Appendix A, Table A6). The number of seeds produced decreased as water level increased (post hoc analysis; Appendix A, Table A7; P-20 cm – 0 cm (WL) = 0.002, P-20 cm – 20 cm (WL) < 0.001, P0 cm – 20 cm (WL) < 0.001). Plants produced fewer seeds in the high salinity treatment than in low or intermediate salinity treatments (P2–18 (SA) < 0.001, P10–18 (SA) < 0.001), and in high than in low nitrogen addition treatments (P0–40 (NA) = 0.028). Plants from corm shoots produced more seeds than those grown from seedlings and plantlets (P < 0.001 in all cases). 4. Discussion Understanding plant environmental niches is crucial for wetland restoration (Zedler, 2000). Our results show that water level and salinity significantly affected the performance of Scirpus mariqueter, and among the three propagule types, corn shoots showed both highest tolerance to flooding stress and highest sexual production. In addition, high nitrogen input inhibited the performance of plants under intermediate salinity conditions. The results obtained here are useful for 4
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Fig. 3. Seed production as influenced by water level (A), salinity (B), nitrogen addition (C) and propagule types. Data shown are means + SE (n = 108 pots). Different lowercase letters denote significant differences among each treatment. Test statistics are in Appendix A: Table A6, A7.
These factors should also be studied, monitored, and managed during restoration.
temperature than in high salinity and intermediate temperature conditions (Przeslawski et al., 2005). Distinct to what has been found in other studies, it is believed that sufficient nitrogen addition can compensate for nutritional imbalances in salt-stressed plants (Gomez et al., 1996; Chen et al., 2010), because salt stress reduces nutrient assimilation in many plant species (Botella et al., 1997; Ehlting et al., 2007). Consequently, caution is needed when selecting nitrogen sources for the restoration of saltmarsh vegetation. Our study also showed that high water levels limited the performance of all three propagule types, and that only corm shoots were able to survive under continuous high water level treatment. This indicates that flooding is the key limiting factor affecting the performance and distribution of these plants (Pennings et al., 2005). Although Scirpus mariqueter is a saltmarsh plant, mainly found in the intertidal zone and can tolerate inundation by tidal water for several hours per day (Roman et al., 1984), persistent inundation can lead to root oxygen deficiency and death (Wang et al., 2010). Inundation can cause physiological problems to plants, including metabolic energy crises in plant cells, carbohydrate deficiency, accumulation of toxic ions, accumulation of harmful metabolites, and decreased water conductivity in roots (Colmer and Voesenek, 2009). In addition to environmental stresses, biological factors such as interspecific competition and herbivory can also affect plant restoration.
4.2. Responses of three types of propagules to environmental factors This study showed that seedlings and plantlets could not survive at a 20 cm water level (i.e., flood conditions). In contrast, corm shoots could survive at this water level, but with restrained growth. Both plantlets and corm shoots exhibited better performance than seedlings in low and intermediate water level treatments. This illustrated that the responses of the three propagule types to environmental stresses differed, that corm shoots were more tolerant of inundation than seedlings and plantlets, and that plantlets were also more tolerant of inundation than seedlings. Plantlets were developed within culture containers with limited light under aseptic conditions on a medium containing ample sugar and nutrients and in an atmosphere with a high level of humidity to allow for heterotrophic growth (Hazarika, 2003; Chandra et al., 2010). They were grown in vessels that had been exposed to an individual microenvironment selected to provide optimum conditions for plant multiplication (Hazarika, 2006). Their adaptability to natural environmental conditions can be weak, particularly if it is exposed to flooding or salinity stress (Hazarika, 2003). Therefore, plantlets can only adapt to certain levels of flooding stress. Salt stress is one of the 5
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Appendix A. Supplementary data
primary abiotic stresses that restrict seed germination and plant growth by inducing ionic and osmotic stress (Liu et al., 2013). Salt and flooding stresses may reduce germination either by limiting water absorption by the seeds, or by influencing the structural organization or composition of proteins in germinating embryos (Almansouri et al., 2001). Therefore, seedlings were the most sensitive to environmental pressures and performed the worst. At lower water levels, the large demand for corms could be reduced if plantlets could be used as propagating material to restore Scirpus mariqueter populations in the field (Adam, 1993). However, planting a single plant or monoclone of the same plant during restoration may be counter-productive (Williams, 2001; Gil et al., 2004; Shen et al., 2007). Studies have shown that genetic diversity has a substantial, positive effect on ecosystem functioning (Kotowska et al., 2010; Cook-Patton et al., 2011; Reusch et al., 2005; Hughes and Stachowicz, 2011). Further studies are needed to assess the impacts of genetic diversity on large-scale field restoration when using plantlets.
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4.3. Implications for restoration Under high water level and high salinity conditions, it is suggested that corms be used to restore Scirpus mariqueter,while seeds are effective propagules under low water levels. Plantlets are also a useful propagule type, particularly at low and intermediate water levels. The effect of nitrogen addition had a minor influence on Scirpus mariqueter and suggested that nitrogen fertilizers be used only in low salinity, intermediate water level restorations. In contrast, under intermediate or high salinity conditions, nitrogen fertilization is not recommended since the interaction of nitrogen addition, salinity, and flooding can adversely affect plant performance. 5. Conclusions Water level was the most important environmental factor limiting the performance of Scirpus mariqueter, and only corm shoots were able to survive under a sustained 20 cm high water level. Salinity stress also limited the performance of Scirpus mariqueter, while the effect of nitrogen addition was not pronounced. In intermediate water level and intermediate salinity treatments, added nitrogen limited the performance of Scirpus mariqueter. In non-flooded saltmarshes, recovery of Scirpus mariqueter can occur at intermediate salinity levels. Based on our experiment, we suggest that the environment niche of corm shoots is broader than seedlings or plantlets and using corm shoots will enhance the success of saltmarsh restoration. We suggest that before large-scale restoration begins, a number of corms with high genetic diversity should be used to expand and produce a large supply of corms. Meanwhile, seeds can be harvested in winter, and then plantlets with high genetic diversity can be used. Therefore, suitable propagators can be selected for restoration, depending on different field environmental conditions. Declaration of Competing Interest The authors declare no competing interests. Acknowledgements We thank Xiaoxing Yang for help in the experiments, and Zhijie Zhang, Xiao Xu, Qicheng Zhong and Shujuan Wei for comments on the manuscript. We also thank Shanghai Chongming Dongtan National Nature Reserve for providing the parts of propagules. This work was supported by the National Key Research and Development Program of China (grant no. 2018YFC1406402), the National Natural Science Foundation of China (grant no. 41630528, 31901228 and 31800411) and the Shanghai Natural Science Foundation of China (Grant Number 17ZR1427400). 6
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Propagule types and environmental stresses matter in saltmarsh plant restoration Qun Zhanga,b, Shiyun Qiua, Yi Zhua,b, Xinhong Cuib, Qiang Hea, Bo Lia,
T
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a
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science, and Institute of Eco-Chongming (IEC), Fudan University, Shanghai 200438, People’s Republic of China b Shanghai Academy of Landscape Architecture Science and Planning, and Shanghai Engineering Research Center of Landscaping on Challenging Urban Sites, NO. 899 Longwu Road, Shanghai 200232, People’s Republic of China
A R T I C LE I N FO
A B S T R A C T
Keywords: Scirpus mariqueter Degraded wetlands Environmental niche Propagules Corm shoots Seedlings Plantlets Population restoration Genetic diversity Synergistic effects
Restoration of degraded saltmarshes has attracted global attention, which makes disentangling the factors that determine target species success critically important. The pioneer plant Scirpus mariqueter in the Yangtze River estuary saltmarshes is rapidly declining due to plant invasion. It needs to be protected and restored, but the effects of environmental factors and propagule types on its restoration success are unclear. We examined the environmental niche of three propagule types (seedlings, corm shoots and plantlets) of Scirpus mariqueter under water level, salinity and nitrogen treatments in a greenhouse experiment. We found that water level was the most critical environmental factor limiting plant performance, followed by salinity. Nitrogen addition inhibited propagule growth in intermediate water level and salinity treatments. There were significant three-way interactions between water level, salinity, and nitrogen addition: Scirpus mariqueter performed best in treatments of low salinity + low to intermediate water levels + high nitrogen. Corm shoots outperformed plantlets and seedlings. Our results suggest that planting corm shoots under intermediate salinity and high water level conditions will enhance the restoration success of Scirpus mariqueter in the saltmarshes of the Yangtze River Estuary.
1. Introduction Saltmarshes are one of the highest valued ecosystems in terms of service provision per unit area (Costanza et al., 1997). They provide valuable services to humans, including the production of materials and food, coastal protection, water purification, carbon sequestration, and education (Barbier et al., 2011; Möller et al., 2014). Nonetheless, human activities such as introduction of invasive plants have led to degradation of these coastal ecosystems globally (Zedler and Kercher, 2005; Bayraktarov et al., 2016). Half of global saltmarshes have been destroyed over the past 50 years, with loss continuing at a rate of 2% each year (Lotze et al., 2006; da Silva Copertino, 2011). Recognition of the potential impact of saltmarsh loss among academics and governmental agencies has led to growing interest in saltmarsh restoration to enhance ecosystem persistence and functioning (Broome et al., 1988; Cronk and Fennessy, 2016). Saltmarsh restoration is complex since restoration goals and targets vary from place to place and degradation involves a range of changes in species abundance and ecosystem functioning (Zedler, 2000). Consequently, saltmarsh restoration presents uncertainties and challenges.
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In practice, vegetation restoration can typically be improved by fertilization, hydrological control and species selection. However, few studies have examined the role of propagule types in restoration success (Seliskar, 1995; Mauchamp et al., 2002; Zhou et al., 2003; Jones et al., 2016). In addition, how differential responses of propagule types to environmental factors impact restoration success is unclear. The availability of viable propagules of target species may also be important (Broome et al., 1988; Mossman et al., 2012). Acquisition of propagules from the wild for restoration may damage to natural populations. Thus, it is important to explore propagule options when restoration target species are limited in large revegetation projects. Tissue culture is an important technique to rapidly obtain plantlet propagules. Whether plantlets perform as effectively as other types of propagules in restorations, however, is unclear. The growth and zonation of saltmarsh plants is related to abiotic factors, including salinity (Chambers et al., 1998; Huckle et al., 2000; Naidoo and Kift, 2006), tidal inundation (Person and Ruess, 2003; Ennis et al., 2014), and nutrient levels (Lohrer and Wetz, 2003; Neves et al., 2010). High soil salinity can prevent seed germination, whereas low soil salinity can promote succession of halophytes to glycophytes
Corresponding author at: Institute of Biodiversity Science, Fudan University, 2005 Songhu Road, Shanghai 200438, People’s Republic of China. E-mail address: [email protected] (B. Li).
https://doi.org/10.1016/j.ecoleng.2019.105693 Received 30 August 2019; Received in revised form 20 November 2019; Accepted 21 November 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.
Ecological Engineering 143 (2020) 105693
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culture dishes in early April 2013 to obtain corm shoots and seedlings. The dishes were placed in a plastic greenhouse with sunlight exposure, at 15–25 °C. Plantlets were obtained from tissue culturing, and the mature seeds of Scirpus mariqueter were used as explants. The procedures of tissue culture contained germ-free germination, induction of multiple shoots, multiplication, rooting and transplanting (Zhang et al., 2016). The common greenhouse experiment was conducted at the Hydrophyte Germplasm Resource Garden in the Shanghai Academy of Landscape Architecture Science and Planning (31° 9′15.7″ N, 121° 26′36.8″ E). The greenhouse was covered with transparent plastic to exclude rainwater, had 45 experimental cement pools and temperature were close to the ambient outdoor conditions.
(Wolters et al., 2005). Inundation can suppress the colonization of some saltmarsh species (Tolley and Christian, 1999), and inundation frequency can affect the dominance of saltmarsh plants (Bockelmann et al., 2002). Increased coastal nitrogen deposition may lead to saltmarsh loss, which reduces ecosystem services provided by saltmarshes (Bertness et al., 2008; Deegan et al., 2012). It is crucial to investigate these effects to maximize salt marsh restoration success. Saltmarshes on Chongming Island in the Yangtze River estuary, Shanghai, China, are important coastal ecosystems (Li et al., 2009). A native species, Scirpus mariqueter, dominates undisturbed saltmarshes as a key species and an ecosystem engineer (Chen et al., 2004). From 2003 to 2014, however, its abundance in Shanghai dropped from 7602 hm2 to less than 550 hm2 largely due to Spartina invasions (Shanghai Chongming Dongtan National Reservec, 2015), and is now threatened with local extinction. The loss of Scirpus mariqueter populations can affect the integrity, ecosystem services, and health of the Yangtze River Estuary (Li et al., 2009). For example, loss of Scirpus mariqueter has reduced various taxa of native biodiversity (Li et al., 2009), especially birds (Gan et al., 2009). Therefore, protection and restoration of this species is needed. To curb further expansion of Spartina alterniflora and restore shorebird habitats, the local government launched a project in 2012 to control Spartina invasion and restore shorebird habitats at Chongming Dongtan. The goals of the project included removal of Spartina, improvement of shorebird habitats and restoration of native plant populations. Presently, the majority of the Spartina alterniflora had been removed to encourage recovery of Scirpus mariqueter (Tang, 2016). However, how different Scirpus mariqueter propagule types respond to environmental factors (i.e. salinity, inundation and nutrient levels) that can inform of restoration success are unclear. This poses the question: how should propagules be selected to maximize population recovery and restoration success? We conducted a greenhouse experiment to examine the environmental niches of three types of propagules of Scirpus mariqueter in different water level, salinity, and nitrogen treatments. Specifically, we addressed the following questions: (1) How do salinity, water level, and nitrogen availability affect the performance of Scirpus mariqueter? and (2) Do the effects of environment factors differ among Scirpus mariqueter propagule types?
2.3. Experimental design Three types of propagules (PR; corm shoots (CS), seedlings (SE), and plantlets (PL)) of similar size (about 10 cm length of each propagule) were selected as experimental materials for the common garden experiment. To make the initial size of the three propagule types as similar as possible, we germinated the seedlings two weeks earlier than corm shoots and plantlets because seedlings grow slower after germination than the others. A fully factorial experimental design was used (Zuur et al., 2009; Harrison et al., 2018), manipulating propagule type and three environmental factors, water level (WL), salinity (SA), and nitrogen addition (NA). Each environmental factor had three levels (−20, 0 and 20 cm to the substrate surface for water level; 2, 10 and 18 g/kg for salinity; 0, 20 and 40 g·m−2·y−1 for nitrogen addition). Water level was referenced to the elevation range in the restoration area and previous experience (Wang et al., 2010); salinity was referenced to the measured value range of water salinity in the restoration area between 2010 and 2012 (1.8–17.8 g/kg) and range of fluctuation of annual mean salinity in natural habitats (Yin et al., 2018); nitrogen addition simulated typical seawater inorganic nitrogen input, the high condition was about 1.6 times of that in Adam Langley et al. (2013), and the range was set according to the results of preliminary experiments. Each treatment combination was replicated four times, resulting in 324 pots (three water levels × three salinity levels × three nitrogen addition levels × three propagules × four replicates). On May 10, 2014, we planted all the propagules in pots (20 cm diameter and 18 cm height) filled with soil collected from the restoration area. In order to ensure one healthy plant per pot, we planted 20 seedlings or 10 corm shoots or 10 plantlets per each pot at beginning, which were then thinned to one focal plant per pot one month after transplantation. We replaced plants that died with new ones during the first two weeks after transplanting. Pots were placed in the 36 cement ponds (100 cm long, 100 cm wide, and 50 cm height with eight small holes in the bottom) with different levels of salinity and nitrogen addition (Appendix Table A1). We placed nine pots (three pots for each of the three types of propagules) into each cement pool. The pools were randomly assigned to one of the three water levels; pots were placed at different heights to achieve different water levels, i.e., −20, 0, and 20 cm. Water was supplied regularly to maintain water level due to evaporation, and salinity was adjusted twice per month. A concentrated nitrogen solution containing equal proportions of ammonium chloride (NH4Cl) and sodium nitrate (NaNO3) was added to the pools fortnightly during the growing season (Ali et al., 2001; Tyler et al., 2007; Ket et al., 2011; Adam Langley et al., 2013). All plants were harvested at the end of September 2014. We counted the ramet number of individuals and the seed number produced per pot. Shoots were cut at the soil surface, and dried at 60–65 °C for three days, while the belowground parts were washed out of the soil using mesh sieves and dried at 60–65 °C for three days. For those pots where all plants died, we set density, seed number, and total biomass as zero.
2. Materials and methods 2.1. Study area The Yangtze estuary is a meso-tidal estuary with semidiurnal tides, and has several alluvial islands, including Hengsha, Changxing and Chongming Islands (Li et al., 2009). Chongming is the oldest and largest of these islands and is the third largest island in China. Geomorphologically, the Yangtze Estuary has a complex structure and provides abundant ecosystem services for human beings and wildlife (Li et al., 2009). Reclamation activities and biological invasion, however, have led to a sharp decline of saltmarshes from 1950s in the estuary (Gu et al., 2018). To prevent range expansion of invasive Spartina alterniflora and restore original habitats, the local government launched a project using integrated methods for invasive plant control and rejuvenation of Scirpus mariqueter and other native species. The project is located in the Chongming Dongtan Bird National Nature Reserve (31°25′~31°38′ N, 121°50′~122°05′ E), on eastern Chongming Island in the Yangtze Estuary (Tang, 2016). 2.2. Propagule materials Corms and seeds of Scirpus mariqueter were collected from ten locations 100 m apart in pure stands of Scirpus mariqueter in the intertidal zone of Chongming Dongtan in the winter of 2012, and stored at 4 °C. Corms or seeds from different locations were mixed and sowed in 2
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Due to the non-normal distribution of data, generalized linear mixed models (GLMMs) were used for examining the effects of water level, salinity, nitrogen addition, and propagule type on plant performance. We used total biomass, density (ramet number per pot), and seed number as response variables. Water level, salinity, nitrogen addition, and propagules were treated as the fixed effects, and ‘pool number’ as a random effect. The GLMMs were analyzed using gamma distribution with the inverse link for total biomass, and the data were (x + 0.001)-transformed (He et al., 2015) to avoid zero values. The effects were tested using likelihood ratio tests (LRT) and the drop1 function in R (Zuur et al., 2009) for GLMMs. Post hoc tests of significant interactions were conducted using the lsmeans function in R (Lenth, 2015; Benítez-Malvido et al., 2018). Where an additive model would explain the data, the significant interactive effects can effectively summarize the main effects in an interpretable way (Lenth, 2012). Furthermore, the results may be misleading due to involvement in interactions. So only the effects of the interaction are presented. The data on density and seed number were analyzed using a Poisson distribution with log link GLMMs, using the GLMMTMB package (Magnusson et al., 2017). For density, the model with four-way interactions did not converge; we therefore included only two- and threeway interactions in the model. For seed number, the models with interactions did not converge, we therefore included only main effects in the model. The significance of effects was tested similarly using the 1 function in R for GLMMs. Post hoc tests of significant interactions were conducted as described above. All analyses were performed with R 3.5.1 (R Development Core Team, 2018).
addition (P < 0.0001, LRT = 57.71; Fig. 1A; Appendix A, Table A2). In the intermediate water level treatment, the total biomass in the intermediate salinity treatment was significantly lower than that in the low salinity treatment only in the high nitrogen addition treatment (post hoc analysis; Appendix A, Table A3; nitrogen addition = 40 g, water level = 0 cm: P2–10 (SA) = 0.004). In the low water level treatment, the total biomass in the intermediate salinity treatment was also significantly lower than the low salinity treatment in the low nitrogen addition treatment (post hoc analysis; Appendix A, Table A3; nitrogen addition = 0 g, water level = −20 cm: P2–10 (SA) = 0.031). However, salinity did not affect the total biomass at low or high water levels, nor in low or intermediate nitrogen addition treatments (P > 0.05 in all cases). In all nitrogen addition × water level treatments, total biomass in the high salinity treatment was significantly lower than in low or intermediate salinity treatments (P < 0.05 in all cases; salinity = 18 g/ kg, total biomass = 0 g), except under the low nitrogen addition and low water level conditions (nitrogen addition = 0 g, water level = −20 cm: P10–18 (SA) = 0.055). Total biomass was also significantly affected by the interaction between water level and propagule type (P < 0.0001, LRT = 379.43; Fig. 1(B); Appendix A, Table A2). In the low water level treatment, the biomass of plants grown from corm shoots was significantly higher than those from seedlings (post hoc analysis; Appendix A, Table A3; water level = −20 cm: PCS-SE(PR) = 0.024). In the intermediate water level treatment, the biomass of plants grown from seedlings was significantly lower than those from both corm shoots and plantlets (water level = 0 cm: PCS-SE(PR) = 0.010, PSE-PL(PR) = 0.018), while in the high water level treatment, total biomass of plants grown from corm shoots was significantly higher than those from both seedlings and plantlets (water level = 20 cm: PCS-SE(PR) < 0.0001, PCS-PL(PR) < 0.0001).
3. Results
3.2. Effects of environmental factors on asexual propagation
3.1. Effects of environmental factors on growth
The density of Scirpus mariqueter decreased as salinity or water level increased (Fig. 2A). Density was also significantly affected by a threeway interaction among salinity, water level, and nitrogen addition (P = .016, LRT = 18.76; Fig. 2A; Appendix A, Table A4). When treated with high nitrogen addition and intermediate water levels, plants under
2.4. Data analysis
The total biomass of Scirpus mariqueter decreased as salinity and water level increased (Fig. 1A), and was also significantly affected by a three-way interaction among salinity, water level, and nitrogen
Fig. 1. A) Total biomass of Scirpus mariqueter in different combinations of water level (−20, 0 and 20 cm), nitrogen addition (0, 20 and 40 g) and salinity (2, 10 and 18 g/kg) treatments. Data shown are means ± SE (n = 12 pots). Different lowercase letters indicate significant differences among three different salinities within the same water level + nitrogen addition treatment combinations. B) Total biomass of three types of propagules in different water level (−20, 0 and 20 cm) treatments. Data shown are means ± SE (n = 36 pots). Different lowercase letters express significant differences among the three types of propagules within the same water level treatment. Test statistics are given in Appendix A: Table A2, A3. Bars without letters illustrate non-significant differences. 3
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Fig. 2. A) Density of Scirpus mariqueter in different combinations of salinity (2, 10 and 18 g/kg), water level (−20, 0 and 20 cm) and nitrogen addition (0, 20 and 40 g) treatments. Data shown are means ± SE (n = 12 pots). Different lowercase letters mean significant differences among three different salinities at the same water level and the same nitrogen addition treatment. B) The density of three types of propagules in different water level (−20, 0 and 20 cm) treatments. Data shown are means ± SE (n = 36 pots). Different lowercase letters show significant differences among the three types of propagules in the same water level treatment. Test statistics are given in Appendix A: Table A4, A5. The bars without letters represent non-significant differences.
informing successful salt marsh restoration.
low salinity treatments exhibited significantly higher densities than plants under intermediate salinity treatments (post hoc analysis; Appendix A, Table A5; nitrogen addition = 40 g, water level = 0 cm: P2–10 (SA) = 0.0001). However, in other nitrogen addition × water level treatments, plants exhibited similar densities at both low and intermediate salinities (P > 0.05 in all cases). Moreover, density was significantly affected by an interaction between water level and propagule type (P < 0.0001, LRT = 201.35; Fig. 2B; Appendix A, Table A4). The pattern of interaction effects on density was similar to that on biomass, and density of plants grown from plantlets was significantly higher than that from seedlings, except in low water level treatments (post hoc analysis; Appendix A, Table A5; water level = −20 cm: PSE - PL (PR) = 0.0005).
4.1. Synergistic effects of environmental factors on plant performance Our study showed that the interaction between high salinity and high water level treatments severely affected the performance of Scirpus mariqueter. All three types of propagules were unable to survive the highest water level and salinity treatments (Figs. 1A, 2A). This is consistent with the results of earlier common garden studies (Huckle et al., 2000; Wang et al., 2010). Previous studies have shown that flooding under saline conditions increased Na+ and Cl− concentrations in shoots, due to increased rates of ion transport (Barrett-Lennard, 2003). These increased concentrations negatively impact plant growth (Barrett-Lennard, 2003). We found that nitrogen addition enhanced the negative effects of salinity on plant performance, but other studies have demonstrated that nitrogen addition can alleviate salinity stress. Our results showed that Scirpus mariqueter performance was significantly affected by an interaction among salinity, water level, and nitrogen addition, and effects on density were broadly similar to those on biomass. In the high nitrogen addition treatment, the intermediate salinity treatment significantly inhibited plant performance, compared with the low salinity treatment, perhaps due to high osmotic pressure in the roots at intermediate salinity levels. Application of nitrate and ammonium increased osmotic pressure of the root system, especially in water-saturated environments, and may promote ion migration (Hessini et al., 2019). Plants experiencing salt stress over the course of several days were highly restricted in their assimilation of nitrate from the nutrient solution, leading these plants to have lower nitrate accumulation in their stems and leaves (Silveira et al., 2001). The salt-osmotic effects evoked by NaCl can damage the root membrane (Maurel et al., 2008), reduce nitrate uptake, restrict nitrates from entering the root xylem (Baki et al., 2000), and reduce the water absorption of plants (Silveira et al., 2001). Such synergistic effects have also been found to occur between grazing and drought, and between salinity and temperature. In drought years, saltmarshes cover was sharp declined with impacts of grazing than in non-drought years (He et al., 2017). Shore molluscs embryonic mortality was significantly higher in response to high salinity in high
3.3. Effects of environmental factors on sexual propagation The number of seeds produced per pot was significantly affected by water level, salinity, nitrogen addition, and propagule type (P < 0.05 in all cases, LRTWL = 49.60, LRTNA = 6.61, LRTPR = 357.71, LRTSA = 40.57; Fig. 3; Appendix A, Table A6). The number of seeds produced decreased as water level increased (post hoc analysis; Appendix A, Table A7; P-20 cm – 0 cm (WL) = 0.002, P-20 cm – 20 cm (WL) < 0.001, P0 cm – 20 cm (WL) < 0.001). Plants produced fewer seeds in the high salinity treatment than in low or intermediate salinity treatments (P2–18 (SA) < 0.001, P10–18 (SA) < 0.001), and in high than in low nitrogen addition treatments (P0–40 (NA) = 0.028). Plants from corm shoots produced more seeds than those grown from seedlings and plantlets (P < 0.001 in all cases). 4. Discussion Understanding plant environmental niches is crucial for wetland restoration (Zedler, 2000). Our results show that water level and salinity significantly affected the performance of Scirpus mariqueter, and among the three propagule types, corn shoots showed both highest tolerance to flooding stress and highest sexual production. In addition, high nitrogen input inhibited the performance of plants under intermediate salinity conditions. The results obtained here are useful for 4
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Fig. 3. Seed production as influenced by water level (A), salinity (B), nitrogen addition (C) and propagule types. Data shown are means + SE (n = 108 pots). Different lowercase letters denote significant differences among each treatment. Test statistics are in Appendix A: Table A6, A7.
These factors should also be studied, monitored, and managed during restoration.
temperature than in high salinity and intermediate temperature conditions (Przeslawski et al., 2005). Distinct to what has been found in other studies, it is believed that sufficient nitrogen addition can compensate for nutritional imbalances in salt-stressed plants (Gomez et al., 1996; Chen et al., 2010), because salt stress reduces nutrient assimilation in many plant species (Botella et al., 1997; Ehlting et al., 2007). Consequently, caution is needed when selecting nitrogen sources for the restoration of saltmarsh vegetation. Our study also showed that high water levels limited the performance of all three propagule types, and that only corm shoots were able to survive under continuous high water level treatment. This indicates that flooding is the key limiting factor affecting the performance and distribution of these plants (Pennings et al., 2005). Although Scirpus mariqueter is a saltmarsh plant, mainly found in the intertidal zone and can tolerate inundation by tidal water for several hours per day (Roman et al., 1984), persistent inundation can lead to root oxygen deficiency and death (Wang et al., 2010). Inundation can cause physiological problems to plants, including metabolic energy crises in plant cells, carbohydrate deficiency, accumulation of toxic ions, accumulation of harmful metabolites, and decreased water conductivity in roots (Colmer and Voesenek, 2009). In addition to environmental stresses, biological factors such as interspecific competition and herbivory can also affect plant restoration.
4.2. Responses of three types of propagules to environmental factors This study showed that seedlings and plantlets could not survive at a 20 cm water level (i.e., flood conditions). In contrast, corm shoots could survive at this water level, but with restrained growth. Both plantlets and corm shoots exhibited better performance than seedlings in low and intermediate water level treatments. This illustrated that the responses of the three propagule types to environmental stresses differed, that corm shoots were more tolerant of inundation than seedlings and plantlets, and that plantlets were also more tolerant of inundation than seedlings. Plantlets were developed within culture containers with limited light under aseptic conditions on a medium containing ample sugar and nutrients and in an atmosphere with a high level of humidity to allow for heterotrophic growth (Hazarika, 2003; Chandra et al., 2010). They were grown in vessels that had been exposed to an individual microenvironment selected to provide optimum conditions for plant multiplication (Hazarika, 2006). Their adaptability to natural environmental conditions can be weak, particularly if it is exposed to flooding or salinity stress (Hazarika, 2003). Therefore, plantlets can only adapt to certain levels of flooding stress. Salt stress is one of the 5
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Appendix A. Supplementary data
primary abiotic stresses that restrict seed germination and plant growth by inducing ionic and osmotic stress (Liu et al., 2013). Salt and flooding stresses may reduce germination either by limiting water absorption by the seeds, or by influencing the structural organization or composition of proteins in germinating embryos (Almansouri et al., 2001). Therefore, seedlings were the most sensitive to environmental pressures and performed the worst. At lower water levels, the large demand for corms could be reduced if plantlets could be used as propagating material to restore Scirpus mariqueter populations in the field (Adam, 1993). However, planting a single plant or monoclone of the same plant during restoration may be counter-productive (Williams, 2001; Gil et al., 2004; Shen et al., 2007). Studies have shown that genetic diversity has a substantial, positive effect on ecosystem functioning (Kotowska et al., 2010; Cook-Patton et al., 2011; Reusch et al., 2005; Hughes and Stachowicz, 2011). Further studies are needed to assess the impacts of genetic diversity on large-scale field restoration when using plantlets.
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4.3. Implications for restoration Under high water level and high salinity conditions, it is suggested that corms be used to restore Scirpus mariqueter,while seeds are effective propagules under low water levels. Plantlets are also a useful propagule type, particularly at low and intermediate water levels. The effect of nitrogen addition had a minor influence on Scirpus mariqueter and suggested that nitrogen fertilizers be used only in low salinity, intermediate water level restorations. In contrast, under intermediate or high salinity conditions, nitrogen fertilization is not recommended since the interaction of nitrogen addition, salinity, and flooding can adversely affect plant performance. 5. Conclusions Water level was the most important environmental factor limiting the performance of Scirpus mariqueter, and only corm shoots were able to survive under a sustained 20 cm high water level. Salinity stress also limited the performance of Scirpus mariqueter, while the effect of nitrogen addition was not pronounced. In intermediate water level and intermediate salinity treatments, added nitrogen limited the performance of Scirpus mariqueter. In non-flooded saltmarshes, recovery of Scirpus mariqueter can occur at intermediate salinity levels. Based on our experiment, we suggest that the environment niche of corm shoots is broader than seedlings or plantlets and using corm shoots will enhance the success of saltmarsh restoration. We suggest that before large-scale restoration begins, a number of corms with high genetic diversity should be used to expand and produce a large supply of corms. Meanwhile, seeds can be harvested in winter, and then plantlets with high genetic diversity can be used. Therefore, suitable propagators can be selected for restoration, depending on different field environmental conditions. Declaration of Competing Interest The authors declare no competing interests. Acknowledgements We thank Xiaoxing Yang for help in the experiments, and Zhijie Zhang, Xiao Xu, Qicheng Zhong and Shujuan Wei for comments on the manuscript. We also thank Shanghai Chongming Dongtan National Nature Reserve for providing the parts of propagules. This work was supported by the National Key Research and Development Program of China (grant no. 2018YFC1406402), the National Natural Science Foundation of China (grant no. 41630528, 31901228 and 31800411) and the Shanghai Natural Science Foundation of China (Grant Number 17ZR1427400). 6
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