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Trait and density responses of Spartina alterniflora to inundation in the Yellow River Delta, China
Marine Pollution Bulletin 146 (2019) 857–864
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Trait and density responses of Spartina alterniflora to inundation in the Yellow River Delta, China
T
Xu Ma, Jiaguo Yan, Fangfang Wang, Dongdong Qiu, Xingpei Jiang, Zezheng Liu, Haochen Sui, ⁎ Junhong Bai, Baoshan Cui State Key Laboratory of Water Environmental Simulation, School of Environment, Beijing NormalUniversity, Beijing 100875, China
ARTICLE INFO
ABSTRACT
Keywords: Inundation Spartina alterniflora Spatial heterogeneity Trait Saltmarsh Yellow River Delta
Understanding plant traits in response to physical stress has been an important issue in the study of coastal saltmarshes. For plants that reproduce both sexually and asexually, whether and how seedlings (sexual reproduction) and clonal ramets (asexual reproduction) may differentially respond to tidal inundation is still unclear. We investigated the growth and morphology of sexual and asexual propagules of an exotic saltmarsh plant (Spartina alterniflora) along a gradient of tidal submergence in the Yellow River Delta. Our results showed that the density, height and basal diameter of clonal ramets or sexual seedlings increased with tidal inundation. The patch amplification edge clonal ramets are superior than patch center plants. The differences response of plants to tidal inundation highlight the sensitivity of S. alterniflora to future tidal regime shifts and can help predict and evaluate the impacts of changes in inundation conditions due to sea level rise, coastal erosion and human activities.
1. Introduction
Different species in salt marshes exhibit high levels of tolerance to abiotic stress factors, particularly tidal flooding (He et al., 2009). Tidal flooding is a challenging environmental stressor and is considered the key factor influencing the distribution and functional traits of salt marsh species. Tidal flooding dynamically alters boundaries and results in spatial heterogeneity, encroachment on ecological niches of native species, and, in turn, intensification of invasion risk (Peterson and Bell, 2012; Hill and Roberts, 2017). The height and duration of tidal flooding are key factors that influence the ranges of tolerance of most salt marsh species, which, in turn, influence vegetation establishment, survival, and expansion through destruction or uprooting (Houwing, 2000; van Katwijk and Hermus, 2000). Spartina alterniflora, a clonal plant, is often observed dominating harsh coastal environments and demonstrates a capacity to span distinct environmental gradients (Vance, 1987; Hartman, 1988; Turkington, 1989; Adam, 1990). In addition, seed bank abundance allows S. alterniflora seeds to germinate in bare tidal flats while sexually propagated seedlings are less likely to be found in such sites due to their low tolerance levels to environmental stress, including tidal flooding (Bertness et al., 1987; Bertness and Shumway, 1992). High inundation levels or long inundation durations inhibit the growth and expansion of species that are sensitive to tidal flooding, and they represent separate unimodal effects of tidal flooding on plant species
Understanding the patterns of plant species distribution and stand characteristics along environmental gradients is a key goal of community ecology (Crain, 2008; Engels et al., 2011; Carus et al., 2017). In tidal estuaries, two abiotic stress gradients are dominant: (1) water and salinity (from the coast to inland, soil salinity gradually increases, and soil moisture content decreases) (Cui et al., 2011b; He et al., 2011, 2012), and (2) the height, duration, and frequency of inundation, in addition to the hydrodynamic forces that form a vertical gradient at each shore location that decrease with an increase in distance from the shore (Proffitt et al., 2003; Engels et al., 2011; Carus et al., 2016). Abiotic stress is a major factor influencing plant distribution patterns and stand characteristics, and it drives vegetation zonation and dynamics in salt marshes (He and Bertness, 2014). Relative tidal height is usually used as an indicator of vegetation zonation in coastal regions. This variable combines the effects of several factors, such as inundation height, inundation duration, and hydrodynamics of waves (Silinski et al., 2015; Silinski et al., 2016; Silinski et al., 2018). Soil salinity, water content, and anaerobic conditions are also potentially influenced by relative tidal height. Therefore, relative average tidal height is a factor influencing plant distribution and community characteristics.
⁎ Corresponding author at: School of Environment, Beijing Normal University, State Key Joint Laboratory of Environmental Simulation and Pollution Control, No. 19 Xinjiekouwai Street, Beijing 100875, China. E-mail address: [email protected] (B. Cui).
https://doi.org/10.1016/j.marpolbul.2019.07.022 Received 12 April 2019; Received in revised form 9 July 2019; Accepted 9 July 2019 Available online 24 July 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
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(Kirwan and Guntenspergen, 2015). However, the effects of tidal flooding on the allometric growth of sexually and asexually reproduced seedlings, particularly in unstable landward patchy areas are poorly understood. Understanding the relationship between S. alterniflora growth and tidal characteristics in patchy areas could facilitate the understanding the invasion of S. alterniflora in tidal environments. S. alterniflora is a typical clonal species found in low salt marshes that gradually invade landward from marsh borders in wetlands in coastal China. Patchy areas with S. alterniflora individuals are in dynamic and unstable states. In the initial stages of S. alterniflora invasions, sparse patches arising from germinating seeds are distributed on the tidal flats. Subsequently, the numbers and area covered by the patches increase, and the number and density of clonal ramets increase gradually and are eventually widespread in low marshes. A large number of irregularly shaped patches are observed in the landward areas. The initial clusters are formed after seed germination and recruitment by asexual reproduction, with their density and the area covered gradually increasing. However, the responses of sexual seedlings or clonal ramets and the community structure to flooding conditions in the unstable invasion landward areas remain unclear. The aim of the present study was to elucidate how flooding patterns influence the growth of invasive plants in salt marshes. The primary objectives were (1) to determine the relationship between S. alterniflora stand characteristics and tidal inundation and (2) to verify whether the left side of the parabolic theory according to Morris et al. (2002) is consistent with the dynamic invasion observed in S. alterniflora. Therefore, we propose the following hypotheses: 1) the above-ground characteristics of S. alterniflora are positively correlated with increasing tidal flooding height; 2) the superiority of clonal ramets at the edge of the patch compared with those in the center of the patch represents the senescence stage in the clone centers and is influenced by tidal flooding height, and 3) sexual seedlings have an optimum range of recruitment that is associated with tidal flooding height. We could predict the development of salt marshes due to sea level rise using the response curves of plant growth and the relationships between spatial variability of vegetation patches and flooding levels.
range. In the S. alterniflora patches, salinity is in the 1.9–7.0 ppt range. The S. alterniflora invasive areas are largely large-scale meadow colonization areas in the low-elevation areas and the patchy colonization areas on both sides of the meadow. The maximum span of the upper patchy area is 800 m. In the area, because of both asexual and sexual reproduction of S. alterniflora, the areas of the patches gradually increase, the plant cover increases, and the hydrological conditions gradually change. 2.2. Field survey In the present study, we focus on S. alterniflora stand characteristics using asexual clonal and sexually propagated seedlings with tidal inundation. We demarcated five large plots perpendicular to the S. alterniflora distribution zones (119°5′ N, 37°49′ E) with spacings of > 50 m, each 50 m (perpendicular to the water's edge) × 100 m (parallel to the water's edge). Each plot consisted of six–eight patch subplots selected randomly, and the patch edge and the patch outer control area were set. We investigated plant growth status of S. alterniflora patches, including sexual reproduction of seeds in the bare mudflats and the asexual reproduction of the colonized patch areas. We collected data on shoot height, shoot diameter in the inner part and the edge, and seedling density in the inner part of each subplot in May, July, and September in 2017. The patchy area with S. alterniflora in the survey site has a long landward extension with a slope < 1‰. The average daily flooding heights among the five large plots surveyed were 6.0–35.5 cm and the daily average maximum tidal heights were 12.2–48.1 cm twice daily. For the determination of soil salinity, the soil inside and outside each patch was obtained using a ring knife, dried at 60 °C, and ground through a 100 mesh sieve. The ratio of soil to water was 1:5. Sedimentation was measured to determine the salinity of the supernatant. 2.3. Inundation level data We set up two Odyssey Flooding height loggers (Z412, New Zealand) in the landward and the seaward direction of the survey plots, and the average flooding heights of the three large plots were obtained based on the differences. The average flooding height of a tidal cycle at the lower elevation area plot was 35.52 cm, and the average flooding height on the land boundary plot was 6.05 cm. The elevation difference between the two sites was 37.9 cm. Based on the integral of the flooding height process line from 0:00 to 24:00 divided by the average time of the day, the time interval was determined to be 10 min.
2. Materials and methods 2.1. Study area Fieldwork was carried out in a salt marsh located in a low elevation saltmarsh area in the Yellow River Delta National Nature Reserve (37°49′ N, 119°05′ E) in northern China (see Fig. 1 in Cui et al., 2011a, 2011b and Fig. 2). The climate is temperate monsoonal, with an average annual precipitation of 537.3 mm and an average annual temperature of 12.88 °C (He et al., 2006). The tides are irregular semidiurnal, with an average tidal amplitude of 1.1–1.5 m (Hu and Cao, 2003). The Yellow River Delta has been artificially planted with S. alterniflora near the No. 5 pile (118°58′ N, 38°0′ E) on the northern side of the Gudong oil exploration site since approximately 1990, and S. alterniflora has spread across the low elevation salt marsh of the Yellow River Delta Nature Reserve over the past few decades and the invasion area exceeded 44 km2 by 2018. The vegetation distribution of the estuary of the Yellow River Delta consists of Japanese eelgrass Zostera japonica, which occupies the subtidal area and S. alterniflora, which occupies the low salt marsh area, and seepweeds Suaeda salsa, which is distributed in the low-high salt marsh area. In addition, five-stamen tamarisk Tamarix chinensis and glasswort Salicornia europaea dominate the terrestrial borders of the salt marshes, and reed Phragmites australis occupy fresh water marshes (Cui et al., 2011a; Cui et al., 2011b; He et al., 2011, 2012; He et al., 2017). The distributions are linked to the tidal coverage area and frequency. The soil salinity of the salt marsh wetland in the Yellow River Delta is in the 1.9–22 ppt range while that of the seawater is in the 14.9–26 ppt
2.4. Statistical analysis All data measured are presented means ± standard deviations throughout the analyses. The significance of the change and singlefactor effects of inundation on the variables were analyzed using oneway analysis of variance (ANOVA) in conjunction with a post hoc Tukey HSD test. The T level of statistical significance was set to P (probability) < 0.05. Relationships between inundation level and S. alterniflora stand characteristics were determined based on the optimal curve-fitting model with the highest coefficient of determination. All analyses of the variables were performed using IBM SPSS 22.0 (IBM, Armonk, NY, US). 3. Results 3.1. Salinity and pH Soil salinity in the S. alterniflora patches was significantly different towards the sea (Fig. 3, a). Salinity gradually decreased with increase in the average flooding height. In addition, soil moisture gradually increased with an increase in flooding height (Fig. 3, b). There were no 858
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Fig. 1. The community distribution pattern of coastal salt marsh in the Yellow River delta.
Fig. 2. (a) The study site at the Yellow River Delta National Nature Reserve, northern China; S. alterniflora patchy area and meadows south of the Gudong oil exploration area; the red line is the patchy area landward boundary, and the white line is the patchy area seaward boundary; the blue line is the tidal creek; the green area is the S. alterniflora distribution area; the black dotted line is the study area with the line transect; (b) S. alterniflora marsh area during inundation; (c) patch center and patch clone amplification region (patch edge) in the subplot survey. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 859
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Fig. 3. (a, b, c) The salinity, moisture and pH (mean + SE) of inner patches and the bare mudflat. Bars with different letters are significantly different.
significant differences of salinity or soil moisture between the inner patches and the bare mudflat. In addition, there were no significant differences in pH along the flooding gradients.
(flooding level = 20.8 cm) at which there was no significant difference. The results also indicate that the flooding conditions influenced the S. alterniflora patches during asexual expansion. In the growing season and in the mature period after May, the enhanced acceleration of plant growth based on height at the edge of the patch was significantly greater than the growth rate of the plants in the inner patches, and a phenomenon of more robust progeny compared to the maternal generation was observed in the breeding strategy. In the growing season, the advantage was most pronounces in the upper land boundary and diminished towards the sea, eventually stabilizing seaward at maturity. In the patchy S. alterniflora distribution area, their heights displayed a gradual increase seaward with an increase in the flooding height and then stabilized in the meadow (inner patches: 76.7–120 cm, patch edges: 93.1–135.8 cm). The clonal ramets at the edges of the patches penetrated the clay surface obliquely during germination and emerged. The basal diameters of the nascent propagules at the edges were significantly larger than the based diameters of the nascent propagules in the inner patches (P < 0.001), excluding the patches where flooding height was > 20.8 cm (Fig. 5, July). In addition, at maturity, the difference gradually increased with an increase in flooding height. The stem diameters of S. alterniflora individuals in the patches were consistent with the flooding height and regularly increased with an increase in flooding height. The basal diameters of the newly emerged S. alterniflora at the edge of the patches were significantly different from the diameters of the newly emerged individuals in the maternal patches. In the early growth stages of S. alterniflora individuals, the basal diameters of the asexually propagated seedlings exhibited a parabolic curve pattern against the flooding level. In the middle of the patchy area (flooding
3.2. Stand characteristics of asexual S. alterniflora propagules along the flooding gradient The heights of the asexual propagules increased significantly with an increase in flooding height seaward. The significant growth in plant growth stage was observed mainly from May to August, and the heights of the asexual propagules at the edge of the patch were significantly higher than the heights of the individuals in the patch center (Fig. 4). In addition, the heights of the asexually propagated individuals in the inner patches were significantly different based on the inundations in different growing seasons (Fig. 4, May: F = 57.168, P < 0.001; July: F = 79.11, P < 0.001; September: F = 60.81, P < 0.001). Neonatal asexual propagules at the edge also were also significantly different based on the inundations in the different seasons. Asexual propagules at the edge in the initial stage of germination (May) are constrained by inundation conditions, which regularly rise and then decrease. The heights on the inner sections and at the edges of the patch were varied in different growth stages. In May, during the germination period of asexual ramets, the heights of the newly emerged asexual ramets amplification were significantly higher at the landward edge than in the maternal plant inner patch (P = 0.017 or P = 0.024). When the flooding height was > 20.8 cm, the plant heights of the newly emerged clonal ramets at the edge were significantly lower than that the heights of the maternal plants in the inner patch (P < 0.001) in the middle of the patchy area (Fig. 4, May). The differences indicate a threshold
Fig. 4. Asexual reproduction height (mean ± SE) at the patch center and edge (red and green lines are the optimal curve-fitting models with the highest coefficients of determination). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 860
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Fig. 5. Asexual seedling diameter (mean ± SE) in the patch center and edge (red and green lines are the optimal curve-fitting models with the highest coefficients of determination). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
level = 20.8 cm), the basal diameters of S. alterniflora individuals were the greatest (7.8 ± 0.45 mm). However, the basal diameters of S. alterniflora individuals gradually increased towards the sea in the later periods regardless of whether the plans were in the inner parts or on the edges. However, the basal diameters of the inner plants increased gradually towards the sea with significant differences between them and the basal diameters of the plants on the outer edges. Notably, the basal diameters of S. alterniflora individuals were initially thick then became narrow afterward in the upper land boundary patches. Different flooding heights, patch locations, and months had significant effects on plant height and stem diameter (Table 1) and there were significant interactive differences between plant height and stem diameter based on flooding height and patch location (F4,1307 = 7.18, P < 0.001, F4,1148 = 9.44, P < 0.001). However, there were no significant differences in patch location and month interactions on stem diameter (F2,1146 = 2.09, P = 0.124).
(F4,102 = 22.83, P < 0.001). In the growth and maturation stages, the plant heights of sexual seedlings exhibited a spatially stable trend with no significant differences (July: F4,90 = 2.80, P = 0.069; September: F4,55 = 1.89, P = 0.159). The average plant heights of annual S. alterniflora seedlings in September were 14.8–19.8 cm. 3.4. Density of sexual and asexual seedlings There was a sparse distribution pattern of S. alterniflora seed germination seedling density towards the sea. The survival rates of the sprouted S. alterniflora seedlings in the patchy area were 6%–42%, and the survival rate gradually increased seaward. Sexually propagated seedlings were widely distributed in mudflats in spring and summer. Due to the low tidal frequency and low inundation height at the land boundary, the seedlings could not germinate. As flooding height increased, seedling density gradually increased to a maximum of 33 ind./ m2 (Fig. 7, a). The overall density of the seedlings showed a decreasing trend with time, and the seedlings colonized only at optimum flooding conditions (< 13.4 cm) with a density of 10.1–13.3 ind./m2. Below this threshold, effective colonization could not occur. As the flooding height increased, the density of asexual clonal ramets gradually increased and eventually stabilized with 398–447 ind./ m2. From May to September, the density increased gradually with the asexual propagation and tillering of individuals (Fig. 7, b).
3.3. Stand characteristics of sexual S. alterniflora propagules along a flooding gradient The heights of sexual seedlings displayed a gradual increase along the inundation gradient in the seedling growth stage (April–May). During the maturation period, sexually propagated seedlings tend to be stable in the open space area. In the early growth stages, the plant heights were mainly 1.67–6.38 cm. Among the different flooding gradients, the heights of sexual seedlings exhibited significant differences
Table 1 Multivariate analysis and statistics on the main effects of stand characteristics. Independent variables are shoot height and stem diameter. The table shows the results from the simplified GLM models for responses of stand characteristics to location (patch center and patch edge), month (May, July, and September) and flooding (N, number of samples; d.f. degrees of freedom; P value, significance of the test (values significant at the 0.05 level are shown in bold)). Source of variation Flooding Location Months Flooding × location Flooding × months Location × months Flooding × location × months
N Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter
d.f.
1304 1145 1304 1145 1304 1145 1304 1145 1304 1145 1304 1145 1304 1145
4 4 1 1 2 2 4 4 8 8 2 2 7 7
861
m.v.
F
P value
11,417 105 9281 359 179,483 9.19 749 17.4 2863 9.85 2741 3.86 133 14.0
109 56.8 88.9 194 1720 4.97 7.18 9.44 27.4 5.33 26.3 2.09 4.27 7.55
< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.007 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.124 0.0021 < 0.001
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4. Discussion
only for the space and resource utilization on a limited spatial scale but also for efficiency and interaction among genes (Proffitt et al., 2003). The expansion of S. alterniflora patches was mainly due to asexual propagules that extend outward through the maternal roots of the patches. The propagules grow rapidly in the initial stages using nutrients supplied by the maternal roots. Our study revealed that in the early growth stages, the differences between the heights of the offspring propagules and the maternal plants changed with an increase in the height of flooding, and the differences were more pronounced at higher flooding levels (Fig. 4). The phenomenon is due to flooding stress, which affects the supply strategies of roots. In the high flooding area, the seedlings emerging directly from the main roots of the parents grow more rapidly to adapt to external stress. In the upper land boundary, the duration of flooding and the height of flooding were lower; therefore, the epitaxial roots of S. alterniflora could grow rapidly using the nutrients supplied by the maternal plant surpass the maternal plants in the patches. The differences in plant height between the progeny and the maternal plants continued to increase later in the course of growth. Regardless of the heights of the flooding, the propagule heights at the patch edges were higher than in the patch center. The phenomenon of the heights of edge nascent propagules being greater than the heights of maternal plants was also observed in stem diameter (Fig. 5). The new edge seedlings were long and thick, while the interior plants were relatively slender. The phenomenon facilitates the development of patches from new seedlings that break through deeper soils and survive. The differences in stem diameter between the progeny and the maternal plants increased with an increase in flooding height, and the differences in plant height were more uniform. According to the authors, the phenomenon is potentially associated with the senescence of clone centers that have been reported by researchers. In addition, the depletion of nutrients has been suggested as a cause of the death observed in clonal plant centers (Ehrenfeld et al., 2005), and the immobilization of nitrogen in alien invaders could lead to their gradual decline (Christian and Wilson, 1999). Some studies do not support the hypothesis that soil nutrient depletion and plant parasitic nematodes or soil pathogens cause aging. Otfinowski et al. (2007) found the loss of clonal viability and plant parasitic or soil pathogens through patch center aging to be irrelevant in invasive clonal plants in Manitoba, Canada, and the soil in the center of the patches also contained higher soil nitrogen, phosphorus, and moisture (Otfinowski et al., 2007). Such aspects of clonal morphology could vary based on plant genotypes and environmental gradients (e.g., elevation), and clonal variations or densities would also result in habitat heterogeneity (Proffitt et al., 2003). The central senescence of S. alterniflora patches could be a function of age-related ramet mortality (Bell, 1974; Harper, 1977), which is potentially independent of the directional growth of rhizomes. However, Proffitt et al. (2003) do not support the hypotrophy hypothesis because the nutrition structure at the patch center is similar to the nutrition structure at the edge (Egerova et al., 2003). In addition, Carteni et al. (2012), Bonanomi et al. (2014) and other researchers propose the hypothesis that the central death or aging observed by cloned species is caused by accumulated negative plant-soil feedback, which decreases the viability of clonal plants (Carteni et al., 2012; Bonanomi et al., 2014). Such problems remain unaddressed due to the accumulation of soil pathogens over time (Derooijvandergoes, 1995) or rust, which are the potential effects of mutualistic fungus (Mitchell et al., 2002; Rudgers et al., 2005). The nutrient supply strategy of the maternal plant and the adaptive strategy of S. alterniflora against flooding height environments jointly influence the existence of the difference phenomenon. Intraspecific competition between genotypes may produce different results at different elevations. The differences between the edge and interior sections of patches are relatively large and enhanced by nutrients supplement between seedlings and ramets, which lead to considerable spatial heterogeneity.
4.1. Stand characteristics of S. alterniflora with flooding gradient According to the results, the relationship between flooding height and plant heights or stem diameters towards the sea mainly indicated that plant heights at the patch center and of the edge nascent propagules increased with an increase in flooding height (Fig. 4). The stem diameters within the patches also increased with an increase in inundation (Fig. 5). The stem diameters of plants at the patch edges exhibited a unimodal relationship with flooding height in the early growth stages and appeared to increase with an increase in flooding height at the mature stages (Fig. 5). In the patchy distribution area, the expansion of patches was mainly based on the clonal ramets produced by the maternal plants. The populations gradually expanded on the mudflat throughout the invasion period, and the patch distribution area extended its unstable dynamic to the land (Morris et al., 2013). The community and stand characteristics would change during the interannual period and eventually achieve a stable state. Morris et al. (2013) proposed the parabolic law of plants under flooding conditions, which is based on a fundamental concept in ecophysiology referred to as the law of tolerance: if a swamp is on the rising side of a parabolic curve and the submersion is below the optimal level, then production would increase with an increase in sea level, while production in a swamp on the falling part on the right side of the curve would decrease with an increase in sea level (Morris et al., 2002). The productivity hump curve achieves the optimal depth with an increase in inundation, and then production decreases with an increase in depth (Morris et al., 2013). Voss et al. (2013), in field experiments, also observed that two large plants, Spartina and Juncus, showed increased growth with increasing inundation during the growing season. The patchy region in the present study was in an unstable state of development with an increase in inundation levels, and the plant heights and diameters of individuals increased, which demonstrated the positive correlation on the left side of Morris' parabola. Large plants such as S. alterniflora have moderately increased their above-ground growth due to rising sea levels (Kirwan and Guntenspergen, 2012). Therefore, the parabolic relationship between plant growth and submergence could reveal whether the swamp would be stable over an extended period of sea level rise (Voss et al., 2013). The conceptual model of the relationship between tidal submergence and above-ground plant growth is the theoretical basis for the evolution and development of salt marshes, which influences the growth and boundary changes of tidal creek networks and estuarine wetlands, and, in turn, influences species distribution, landscape patterns, and species movements (Moody and Aronson, 2007; Kirwan et al., 2012; Carus et al., 2017). Numerous studies have described the significant correlation between interannual sea level and above-ground biomass and elucidated the close relationship between stand characteristics and sea level (Silinski et al., 2016; Hill and Roberts, 2017; Gittman et al., 2018; Li et al., 2018). The proposed feedback of the parabolic relationship is applicable in relatively stable salt marshes characterized by regular tidal and rich sediments, and a similar relationship is equally applicable in unstable saltmarshes that are undergoing invasion. Alternatively, at low elevations or under rapid rates of sea level rise, increases in inundation decrease vegetation growth and lead to the rapid submergence of marshes. Therefore, a parabolic relationship between plant growth and inundation could potentially explain whether a marsh would be stable for thousands of years or whether it would be submerged rapidly (Morris et al., 2002). 4.2. Advantages of offspring propagules over maternal plants We observed that offspring clonal ramets had some advantages over maternal plants based on stand characteristics between the center and the edges of the patches (Fig. 4 and Fig. 5). This finding is critical not 862
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morphometric quantities and salinity stress in S. alterniflora could be due to increased physiological and anatomical specialization, or could reflect the adaptation of genotypes to other stress factors in addition to salinity (Hester et al., 1998). The elevation relative to the average flooding height is often used as a general indicator of the distribution patterns of species along environmental gradients. In the present study, we use inundation height, a predictable variable that directly influences plant growth, instead of elevation, as a surrogate factor for functionally linked variable effects. Proffitt et al. (2003) reported that seedlings have a wide range of sexual reproduction output, with an average of 24.2 seedlings/m2, with similar rates of emergence in low-elevation areas and high-elevation areas (Proffitt et al., 2003), which was inconsistent with the findings of the present study. In May, during the seedling stage, the seedling emergence rate was low due to the minimal tidal disturbance or high salinity stress at higher elevations. The intervals of survival and adaptation of sexual propagules in the flooding regime is an important reason to determine the population distribution of S. alterniflora. This is an important indicator threshold for evaluating the spreading capacity of the population. Our results confirm that in the extensive estuarine wetlands, the S. alterniflora growth is limited by elevation.
Fig. 6. Heights of sexually (mean ± SE) propagated S. alterniflora seedlings on the bare mudflat. Bars with different letters are significantly different.
4.3. Inundation height adaptation threshold for sexual propagules of S. alterniflora
5. Conclusions
Colonization by sexual propagules has an adaptive flooding height threshold. The emergence rate of seedlings increases with an increase in flooding height and gradually stabilizes at a flooding height of 13–38 cm (Fig. 6), with an average of 3.6–10 seedlings/m2 (Fig. 7). The germination of sexual propagules, seedling supplementation, and subsequent clonal propagation were critical for the expansion of the S. alterniflora populations. Colonization by sexual propagules is a dynamic process that influences the development of patchy areas and is often underestimated. The land boundary in our study area had a high evaporation rate and a relatively low tidal frequency disturbance due to its higher elevation, making salinity higher than in the low elevation area. We conclude that the lower tidal frequency and high salinity or low soil moisture content stress are the major reasons why sexual propagules cannot colonize the higher tide areas of the Yellow River Delta. Although numerous morphological and growth traits are under the influence of genetic control some extent, many are clearly influenced by environmental factors such as elevation (Proffitt et al., 2003). According to Hester et al. (1998), the lack of correlation between
Based on the parabolic relationship between plant productivity and submergent conditions described in Morris et al. (2002), we propose a positive correlation between the above-ground characteristics of S. alterniflora and inundation in an unstable invasive dynamic zone, which is consistent with the correlation suggested for the left side of the parabola in Morris et al. (2002). The interannual variability of tidal inundation conditions would influence the dynamic changes to the boundary of the invasion area. The positive relationship between the stand characteristics and tidal inundation facilitates the gradual expansion of patches that influence tidal networks, interspecific competition, and habitat heterogeneity. To facilitate long-term observations of plant growth and interannual flooding conditions in dynamic invading areas, it is critical to understand the dynamic processes of invasion. It is also important to establish a numerical models for stand characteristics–inundation condition–sedimentary erosion feedback effects on S. alterniflora, which could facilitate the proper assessment and prediction of the impacts of changes in tidal conditions on S. alterniflora invasion linked to sea-level rise, coastal erosion, and human activities.
Fig. 7. The density of sexual (mean + SE) and asexual clone seedlings (mean ± SE) of S. alterniflora. Bars with different letters are significantly different. 863
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Author contributions
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Peterson, J.M., Bell, S.S., 2012. Tidal events and salt-marsh structure influence black mangrove (Avicennia germinans) recruitment across an ecotone. Ecology 93, 1648–1658. https://doi.org/10.1890/11-1430.1. Proffitt, C.E., Travis, S.E., Edwards, K.R., 2003. Genotype and elevation influence Spartina alterniflora colonization and growth in a created salt marsh. Ecol. Appl. 13, 180–192. https://doi.org/10.1890/1051-0761(2003)013[0180:Gaeisa]2.0.Co;2. Rudgers, J.A., Mattingly, W.B., Koslow, J.M., 2005. Mutualistic fungus promotes plant invasion into diverse communities. Oecologia 144, 463–471. https://doi.org/10. 1007/s00442-005-0039-y. Silinski, A., Heuner, M., Schoelynck, J., Puijalon, S., Schroder, U., Fuchs, E., Troch, P., Bouma, T.J., Meire, P., Temmerman, S., 2015. Effects of wind waves versus ship waves on tidal marsh plants: a flume study on different life stages of Scirpus maritimus. PLoS One 10, e0118687. https://doi.org/10.1371/journal.pone.0118687. Silinski, A., van Belzen, J., Fransen, E., Bouma, T.J., Troch, P., Meire, P., Temmerman, S., 2016. Quantifying critical conditions for seaward expansion of tidal marshes: a transplantation experiment. Estuar. Coast. Shelf Sci. 169, 227–237. https://doi.org/ 10.1016/j.ecss.2015.12.012. Silinski, A., Schoutens, K., Puijalon, S., Schoelynck, J., Luyckx, D., Troch, P., Meire, P., Temmerman, S., 2018. Coping with waves: plasticity in tidal marsh plants as selfadapting coastal ecosystem engineers. Limnol. Oceanogr. 63, 799–815. https://doi. org/10.1002/lno.10671. Turkington, R., 1989. The growth, distribution and neighbor relationships of TrifoliumRepens in a permanent pasture. 5. The coevolution of competitors. J. Ecol. 77, 717–733. https://doi.org/10.2307/2260981. van Katwijk, M.M., Hermus, D.C.R., 2000. Effects of water dynamics on Zostera marina: transplantation experiments in the intertidal Dutch Wadden Sea. Mar. Ecol. Prog. Ser. 208, 107–118. https://doi.org/10.3354/meps208107. Vance, R.R., 1987. Population biology and evolution of clonal organisms - Jackson,Jbc, Buss,Lw, Cook,Re. Science 235, 1264. https://doi.org/10.1126/science.235.4793. 1264. Voss, C.M., Christian, R.R., Morris, J.T., 2013. Marsh macrophyte responses to inundation anticipate impacts of sea-level rise and indicate ongoing drowning of North Carolina marshes. Mar. Biol. 160, 181–194. https://doi.org/10.1007/s00227-012-2076-5.
Xu Ma designed the study and performed a field plot survey; Xingpei Jiang, Fangfang Wang and Haochen Sui performed a part of the field experiment; Xu Ma analyzed the data; Xu Ma and Baoshan Cui wrote the manuscript; Jiaguo Yan and other authors contributed revisions and suggestions to the manuscript. Acknowledgements The study was supported financially by the Key Project of the National Natural Science Foundation of China (51639001), the Fund for Innovative Research Group of the National Natural Science Foundation of China (51721093), the Key Consulting Project of Chinese Academy of Engineering (2018-XZ-14). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.marpolbul.2019.07.022. References Adam, P., 1990. Saltmarsh Ecology. Cambridge University Press, Cambridge ; New York. Bell, A.D., 1974. Rhizome organization in relation to vegetative spread in MedeolaVirginiana. J. Arnold Arboretum 55, 458–468. Bertness, M.D., Shumway, S.W., 1992. Consumer driven pollen limitation of seed production in marsh grasses. Am. J. Bot. 79, 288–293. https://doi.org/10.2307/ 2445017. Bertness, M.D., Wise, C., Ellison, A.M., 1987. Consumer pressure and seed set in a saltmarsh perennial plant community. Oecologia 71, 190–200. https://doi.org/10.1007/ Bf00377284. Bonanomi, G., Incerti, G., Stinca, A., Carteni, F., Giannino, F., Mazzoleni, S., 2014. Ring formation in clonal plants. Community Ecol. 15, 77–86. https://doi.org/10.1556/ Comec.15.2014.1.8. Carteni, F., Marasco, A., Bonanomi, G., Mazzoleni, S., Rietkerk, M., Giannino, F., 2012. Negative plant soil feedback explaining ring formation in clonal plants. J. Theor. Biol. 313, 153–161. https://doi.org/10.1016/j.jtbi.2012.08.008. Carus, J., Paul, M., Schroder, B., 2016. Vegetation as self-adaptive coastal protection: reduction of current velocity and morphologic plasticity of a brackish marsh pioneer. Ecol. Evol. 6, 1579–1589. https://doi.org/10.1002/ece3.1904. Carus, J., Heuner, M., Paul, M., Schroder, B., 2017. Plant distribution and stand characteristics in brackish marshes: unravelling the roles of abiotic factors and interspecific competition. Estuar. Coast. Shelf Sci. 196, 237–247. https://doi.org/10. 1016/j.ecss.2017.06.038. Christian, J.M., Wilson, S.D., 1999. Long-term ecosystem impacts of an introduced grass in the northern Great Plains. Ecology 80, 2397–2407. https://doi.org/10.2307/ 176919. Crain, C.M., 2008. Interactions between marsh plant species vary in direction and strength depending on environmental and consumer context. J. Ecol. 96, 166–173. https://doi.org/10.1111/j.1365-2745.2007.01314.x. Cui, B.S., He, Q., Zhang, K.J., Chen, X., 2011a. Determinants of annual-perennial plant zonation across a salt-fresh marsh interface: a multistage assessment. Oecologia 166, 1067–1075. https://doi.org/10.1007/s00442-011-1944-x. Cui, B.S., He, Q.A., An, Y.A., 2011b. Community structure and abiotic determinants of salt marsh plant zonation vary across topographic gradients. Estuar. Coasts 34, 459–469. https://doi.org/10.1007/s12237-010-9364-4. Derooijvandergoes, P.C.E.M., 1995. The role of plant-parasitic nematodes and soil-borne fungi in the decline of Ammophila-Arenaria (L) link. New Phytol. 129, 661–669. Egerova, J., Proffitt, C.E., Travis, S.E., 2003. Facilitation of survival and growth of Baccharis halimifolia L. by Spartina alterniflora Loisel. in a created Louisiana salt marsh. Wetlands 23, 250–256. https://doi.org/10.1672/4-20. Ehrenfeld, J.G., Ravit, B., Elgersma, K., 2005. Feedback in the plant-soil system. Annu. Rev. Environ. Resour. 30, 75–115. https://doi.org/10.1146/annurev.energy.30. 050504.144212. Engels, J.G., Rink, F., Jensen, K., 2011. Stress tolerance and biotic interactions determine plant zonation patterns in estuarine marshes during seedling emergence and early establishment. J. Ecol. 99, 277–287. https://doi.org/10.1111/j.1365-2745.2010. 01745.x. Gittman, R.K., Fodrie, F.J., Baillie, C.J., Brodeur, M.C., Currin, C.A., Keller, D.A., Kenworthy, M.D., Morton, J.P., Ridge, J.T., Zhang, Y.S., 2018. Living on the edge: increasing patch size enhances the resilience and community development of a restored salt marsh. Estuar. Coasts 41, 884–895. https://doi.org/10.1007/s12237-0170302-6. Harper, J.L., 1977. Population Biology of Plants. Academic Press, London; New York. Hartman, J.M., 1988. Recolonization of small disturbance patches in a New-England saltmarsh. Am. J. Bot. 75, 1625–1631. https://doi.org/10.2307/2444678. He, Q., Bertness, M.D., 2014. Extreme stresses, niches, and positive species interactions along stress gradients. Ecology 95, 1437–1443. https://doi.org/10.1890/13-2226.1.
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Trait and density responses of Spartina alterniflora to inundation in the Yellow River Delta, China
T
Xu Ma, Jiaguo Yan, Fangfang Wang, Dongdong Qiu, Xingpei Jiang, Zezheng Liu, Haochen Sui, ⁎ Junhong Bai, Baoshan Cui State Key Laboratory of Water Environmental Simulation, School of Environment, Beijing NormalUniversity, Beijing 100875, China
ARTICLE INFO
ABSTRACT
Keywords: Inundation Spartina alterniflora Spatial heterogeneity Trait Saltmarsh Yellow River Delta
Understanding plant traits in response to physical stress has been an important issue in the study of coastal saltmarshes. For plants that reproduce both sexually and asexually, whether and how seedlings (sexual reproduction) and clonal ramets (asexual reproduction) may differentially respond to tidal inundation is still unclear. We investigated the growth and morphology of sexual and asexual propagules of an exotic saltmarsh plant (Spartina alterniflora) along a gradient of tidal submergence in the Yellow River Delta. Our results showed that the density, height and basal diameter of clonal ramets or sexual seedlings increased with tidal inundation. The patch amplification edge clonal ramets are superior than patch center plants. The differences response of plants to tidal inundation highlight the sensitivity of S. alterniflora to future tidal regime shifts and can help predict and evaluate the impacts of changes in inundation conditions due to sea level rise, coastal erosion and human activities.
1. Introduction
Different species in salt marshes exhibit high levels of tolerance to abiotic stress factors, particularly tidal flooding (He et al., 2009). Tidal flooding is a challenging environmental stressor and is considered the key factor influencing the distribution and functional traits of salt marsh species. Tidal flooding dynamically alters boundaries and results in spatial heterogeneity, encroachment on ecological niches of native species, and, in turn, intensification of invasion risk (Peterson and Bell, 2012; Hill and Roberts, 2017). The height and duration of tidal flooding are key factors that influence the ranges of tolerance of most salt marsh species, which, in turn, influence vegetation establishment, survival, and expansion through destruction or uprooting (Houwing, 2000; van Katwijk and Hermus, 2000). Spartina alterniflora, a clonal plant, is often observed dominating harsh coastal environments and demonstrates a capacity to span distinct environmental gradients (Vance, 1987; Hartman, 1988; Turkington, 1989; Adam, 1990). In addition, seed bank abundance allows S. alterniflora seeds to germinate in bare tidal flats while sexually propagated seedlings are less likely to be found in such sites due to their low tolerance levels to environmental stress, including tidal flooding (Bertness et al., 1987; Bertness and Shumway, 1992). High inundation levels or long inundation durations inhibit the growth and expansion of species that are sensitive to tidal flooding, and they represent separate unimodal effects of tidal flooding on plant species
Understanding the patterns of plant species distribution and stand characteristics along environmental gradients is a key goal of community ecology (Crain, 2008; Engels et al., 2011; Carus et al., 2017). In tidal estuaries, two abiotic stress gradients are dominant: (1) water and salinity (from the coast to inland, soil salinity gradually increases, and soil moisture content decreases) (Cui et al., 2011b; He et al., 2011, 2012), and (2) the height, duration, and frequency of inundation, in addition to the hydrodynamic forces that form a vertical gradient at each shore location that decrease with an increase in distance from the shore (Proffitt et al., 2003; Engels et al., 2011; Carus et al., 2016). Abiotic stress is a major factor influencing plant distribution patterns and stand characteristics, and it drives vegetation zonation and dynamics in salt marshes (He and Bertness, 2014). Relative tidal height is usually used as an indicator of vegetation zonation in coastal regions. This variable combines the effects of several factors, such as inundation height, inundation duration, and hydrodynamics of waves (Silinski et al., 2015; Silinski et al., 2016; Silinski et al., 2018). Soil salinity, water content, and anaerobic conditions are also potentially influenced by relative tidal height. Therefore, relative average tidal height is a factor influencing plant distribution and community characteristics.
⁎ Corresponding author at: School of Environment, Beijing Normal University, State Key Joint Laboratory of Environmental Simulation and Pollution Control, No. 19 Xinjiekouwai Street, Beijing 100875, China. E-mail address: [email protected] (B. Cui).
https://doi.org/10.1016/j.marpolbul.2019.07.022 Received 12 April 2019; Received in revised form 9 July 2019; Accepted 9 July 2019 Available online 24 July 2019 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.
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(Kirwan and Guntenspergen, 2015). However, the effects of tidal flooding on the allometric growth of sexually and asexually reproduced seedlings, particularly in unstable landward patchy areas are poorly understood. Understanding the relationship between S. alterniflora growth and tidal characteristics in patchy areas could facilitate the understanding the invasion of S. alterniflora in tidal environments. S. alterniflora is a typical clonal species found in low salt marshes that gradually invade landward from marsh borders in wetlands in coastal China. Patchy areas with S. alterniflora individuals are in dynamic and unstable states. In the initial stages of S. alterniflora invasions, sparse patches arising from germinating seeds are distributed on the tidal flats. Subsequently, the numbers and area covered by the patches increase, and the number and density of clonal ramets increase gradually and are eventually widespread in low marshes. A large number of irregularly shaped patches are observed in the landward areas. The initial clusters are formed after seed germination and recruitment by asexual reproduction, with their density and the area covered gradually increasing. However, the responses of sexual seedlings or clonal ramets and the community structure to flooding conditions in the unstable invasion landward areas remain unclear. The aim of the present study was to elucidate how flooding patterns influence the growth of invasive plants in salt marshes. The primary objectives were (1) to determine the relationship between S. alterniflora stand characteristics and tidal inundation and (2) to verify whether the left side of the parabolic theory according to Morris et al. (2002) is consistent with the dynamic invasion observed in S. alterniflora. Therefore, we propose the following hypotheses: 1) the above-ground characteristics of S. alterniflora are positively correlated with increasing tidal flooding height; 2) the superiority of clonal ramets at the edge of the patch compared with those in the center of the patch represents the senescence stage in the clone centers and is influenced by tidal flooding height, and 3) sexual seedlings have an optimum range of recruitment that is associated with tidal flooding height. We could predict the development of salt marshes due to sea level rise using the response curves of plant growth and the relationships between spatial variability of vegetation patches and flooding levels.
range. In the S. alterniflora patches, salinity is in the 1.9–7.0 ppt range. The S. alterniflora invasive areas are largely large-scale meadow colonization areas in the low-elevation areas and the patchy colonization areas on both sides of the meadow. The maximum span of the upper patchy area is 800 m. In the area, because of both asexual and sexual reproduction of S. alterniflora, the areas of the patches gradually increase, the plant cover increases, and the hydrological conditions gradually change. 2.2. Field survey In the present study, we focus on S. alterniflora stand characteristics using asexual clonal and sexually propagated seedlings with tidal inundation. We demarcated five large plots perpendicular to the S. alterniflora distribution zones (119°5′ N, 37°49′ E) with spacings of > 50 m, each 50 m (perpendicular to the water's edge) × 100 m (parallel to the water's edge). Each plot consisted of six–eight patch subplots selected randomly, and the patch edge and the patch outer control area were set. We investigated plant growth status of S. alterniflora patches, including sexual reproduction of seeds in the bare mudflats and the asexual reproduction of the colonized patch areas. We collected data on shoot height, shoot diameter in the inner part and the edge, and seedling density in the inner part of each subplot in May, July, and September in 2017. The patchy area with S. alterniflora in the survey site has a long landward extension with a slope < 1‰. The average daily flooding heights among the five large plots surveyed were 6.0–35.5 cm and the daily average maximum tidal heights were 12.2–48.1 cm twice daily. For the determination of soil salinity, the soil inside and outside each patch was obtained using a ring knife, dried at 60 °C, and ground through a 100 mesh sieve. The ratio of soil to water was 1:5. Sedimentation was measured to determine the salinity of the supernatant. 2.3. Inundation level data We set up two Odyssey Flooding height loggers (Z412, New Zealand) in the landward and the seaward direction of the survey plots, and the average flooding heights of the three large plots were obtained based on the differences. The average flooding height of a tidal cycle at the lower elevation area plot was 35.52 cm, and the average flooding height on the land boundary plot was 6.05 cm. The elevation difference between the two sites was 37.9 cm. Based on the integral of the flooding height process line from 0:00 to 24:00 divided by the average time of the day, the time interval was determined to be 10 min.
2. Materials and methods 2.1. Study area Fieldwork was carried out in a salt marsh located in a low elevation saltmarsh area in the Yellow River Delta National Nature Reserve (37°49′ N, 119°05′ E) in northern China (see Fig. 1 in Cui et al., 2011a, 2011b and Fig. 2). The climate is temperate monsoonal, with an average annual precipitation of 537.3 mm and an average annual temperature of 12.88 °C (He et al., 2006). The tides are irregular semidiurnal, with an average tidal amplitude of 1.1–1.5 m (Hu and Cao, 2003). The Yellow River Delta has been artificially planted with S. alterniflora near the No. 5 pile (118°58′ N, 38°0′ E) on the northern side of the Gudong oil exploration site since approximately 1990, and S. alterniflora has spread across the low elevation salt marsh of the Yellow River Delta Nature Reserve over the past few decades and the invasion area exceeded 44 km2 by 2018. The vegetation distribution of the estuary of the Yellow River Delta consists of Japanese eelgrass Zostera japonica, which occupies the subtidal area and S. alterniflora, which occupies the low salt marsh area, and seepweeds Suaeda salsa, which is distributed in the low-high salt marsh area. In addition, five-stamen tamarisk Tamarix chinensis and glasswort Salicornia europaea dominate the terrestrial borders of the salt marshes, and reed Phragmites australis occupy fresh water marshes (Cui et al., 2011a; Cui et al., 2011b; He et al., 2011, 2012; He et al., 2017). The distributions are linked to the tidal coverage area and frequency. The soil salinity of the salt marsh wetland in the Yellow River Delta is in the 1.9–22 ppt range while that of the seawater is in the 14.9–26 ppt
2.4. Statistical analysis All data measured are presented means ± standard deviations throughout the analyses. The significance of the change and singlefactor effects of inundation on the variables were analyzed using oneway analysis of variance (ANOVA) in conjunction with a post hoc Tukey HSD test. The T level of statistical significance was set to P (probability) < 0.05. Relationships between inundation level and S. alterniflora stand characteristics were determined based on the optimal curve-fitting model with the highest coefficient of determination. All analyses of the variables were performed using IBM SPSS 22.0 (IBM, Armonk, NY, US). 3. Results 3.1. Salinity and pH Soil salinity in the S. alterniflora patches was significantly different towards the sea (Fig. 3, a). Salinity gradually decreased with increase in the average flooding height. In addition, soil moisture gradually increased with an increase in flooding height (Fig. 3, b). There were no 858
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Fig. 1. The community distribution pattern of coastal salt marsh in the Yellow River delta.
Fig. 2. (a) The study site at the Yellow River Delta National Nature Reserve, northern China; S. alterniflora patchy area and meadows south of the Gudong oil exploration area; the red line is the patchy area landward boundary, and the white line is the patchy area seaward boundary; the blue line is the tidal creek; the green area is the S. alterniflora distribution area; the black dotted line is the study area with the line transect; (b) S. alterniflora marsh area during inundation; (c) patch center and patch clone amplification region (patch edge) in the subplot survey. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 859
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Fig. 3. (a, b, c) The salinity, moisture and pH (mean + SE) of inner patches and the bare mudflat. Bars with different letters are significantly different.
significant differences of salinity or soil moisture between the inner patches and the bare mudflat. In addition, there were no significant differences in pH along the flooding gradients.
(flooding level = 20.8 cm) at which there was no significant difference. The results also indicate that the flooding conditions influenced the S. alterniflora patches during asexual expansion. In the growing season and in the mature period after May, the enhanced acceleration of plant growth based on height at the edge of the patch was significantly greater than the growth rate of the plants in the inner patches, and a phenomenon of more robust progeny compared to the maternal generation was observed in the breeding strategy. In the growing season, the advantage was most pronounces in the upper land boundary and diminished towards the sea, eventually stabilizing seaward at maturity. In the patchy S. alterniflora distribution area, their heights displayed a gradual increase seaward with an increase in the flooding height and then stabilized in the meadow (inner patches: 76.7–120 cm, patch edges: 93.1–135.8 cm). The clonal ramets at the edges of the patches penetrated the clay surface obliquely during germination and emerged. The basal diameters of the nascent propagules at the edges were significantly larger than the based diameters of the nascent propagules in the inner patches (P < 0.001), excluding the patches where flooding height was > 20.8 cm (Fig. 5, July). In addition, at maturity, the difference gradually increased with an increase in flooding height. The stem diameters of S. alterniflora individuals in the patches were consistent with the flooding height and regularly increased with an increase in flooding height. The basal diameters of the newly emerged S. alterniflora at the edge of the patches were significantly different from the diameters of the newly emerged individuals in the maternal patches. In the early growth stages of S. alterniflora individuals, the basal diameters of the asexually propagated seedlings exhibited a parabolic curve pattern against the flooding level. In the middle of the patchy area (flooding
3.2. Stand characteristics of asexual S. alterniflora propagules along the flooding gradient The heights of the asexual propagules increased significantly with an increase in flooding height seaward. The significant growth in plant growth stage was observed mainly from May to August, and the heights of the asexual propagules at the edge of the patch were significantly higher than the heights of the individuals in the patch center (Fig. 4). In addition, the heights of the asexually propagated individuals in the inner patches were significantly different based on the inundations in different growing seasons (Fig. 4, May: F = 57.168, P < 0.001; July: F = 79.11, P < 0.001; September: F = 60.81, P < 0.001). Neonatal asexual propagules at the edge also were also significantly different based on the inundations in the different seasons. Asexual propagules at the edge in the initial stage of germination (May) are constrained by inundation conditions, which regularly rise and then decrease. The heights on the inner sections and at the edges of the patch were varied in different growth stages. In May, during the germination period of asexual ramets, the heights of the newly emerged asexual ramets amplification were significantly higher at the landward edge than in the maternal plant inner patch (P = 0.017 or P = 0.024). When the flooding height was > 20.8 cm, the plant heights of the newly emerged clonal ramets at the edge were significantly lower than that the heights of the maternal plants in the inner patch (P < 0.001) in the middle of the patchy area (Fig. 4, May). The differences indicate a threshold
Fig. 4. Asexual reproduction height (mean ± SE) at the patch center and edge (red and green lines are the optimal curve-fitting models with the highest coefficients of determination). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 860
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Fig. 5. Asexual seedling diameter (mean ± SE) in the patch center and edge (red and green lines are the optimal curve-fitting models with the highest coefficients of determination). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
level = 20.8 cm), the basal diameters of S. alterniflora individuals were the greatest (7.8 ± 0.45 mm). However, the basal diameters of S. alterniflora individuals gradually increased towards the sea in the later periods regardless of whether the plans were in the inner parts or on the edges. However, the basal diameters of the inner plants increased gradually towards the sea with significant differences between them and the basal diameters of the plants on the outer edges. Notably, the basal diameters of S. alterniflora individuals were initially thick then became narrow afterward in the upper land boundary patches. Different flooding heights, patch locations, and months had significant effects on plant height and stem diameter (Table 1) and there were significant interactive differences between plant height and stem diameter based on flooding height and patch location (F4,1307 = 7.18, P < 0.001, F4,1148 = 9.44, P < 0.001). However, there were no significant differences in patch location and month interactions on stem diameter (F2,1146 = 2.09, P = 0.124).
(F4,102 = 22.83, P < 0.001). In the growth and maturation stages, the plant heights of sexual seedlings exhibited a spatially stable trend with no significant differences (July: F4,90 = 2.80, P = 0.069; September: F4,55 = 1.89, P = 0.159). The average plant heights of annual S. alterniflora seedlings in September were 14.8–19.8 cm. 3.4. Density of sexual and asexual seedlings There was a sparse distribution pattern of S. alterniflora seed germination seedling density towards the sea. The survival rates of the sprouted S. alterniflora seedlings in the patchy area were 6%–42%, and the survival rate gradually increased seaward. Sexually propagated seedlings were widely distributed in mudflats in spring and summer. Due to the low tidal frequency and low inundation height at the land boundary, the seedlings could not germinate. As flooding height increased, seedling density gradually increased to a maximum of 33 ind./ m2 (Fig. 7, a). The overall density of the seedlings showed a decreasing trend with time, and the seedlings colonized only at optimum flooding conditions (< 13.4 cm) with a density of 10.1–13.3 ind./m2. Below this threshold, effective colonization could not occur. As the flooding height increased, the density of asexual clonal ramets gradually increased and eventually stabilized with 398–447 ind./ m2. From May to September, the density increased gradually with the asexual propagation and tillering of individuals (Fig. 7, b).
3.3. Stand characteristics of sexual S. alterniflora propagules along a flooding gradient The heights of sexual seedlings displayed a gradual increase along the inundation gradient in the seedling growth stage (April–May). During the maturation period, sexually propagated seedlings tend to be stable in the open space area. In the early growth stages, the plant heights were mainly 1.67–6.38 cm. Among the different flooding gradients, the heights of sexual seedlings exhibited significant differences
Table 1 Multivariate analysis and statistics on the main effects of stand characteristics. Independent variables are shoot height and stem diameter. The table shows the results from the simplified GLM models for responses of stand characteristics to location (patch center and patch edge), month (May, July, and September) and flooding (N, number of samples; d.f. degrees of freedom; P value, significance of the test (values significant at the 0.05 level are shown in bold)). Source of variation Flooding Location Months Flooding × location Flooding × months Location × months Flooding × location × months
N Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter Shoot height Stem diameter
d.f.
1304 1145 1304 1145 1304 1145 1304 1145 1304 1145 1304 1145 1304 1145
4 4 1 1 2 2 4 4 8 8 2 2 7 7
861
m.v.
F
P value
11,417 105 9281 359 179,483 9.19 749 17.4 2863 9.85 2741 3.86 133 14.0
109 56.8 88.9 194 1720 4.97 7.18 9.44 27.4 5.33 26.3 2.09 4.27 7.55
< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.007 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 0.124 0.0021 < 0.001
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4. Discussion
only for the space and resource utilization on a limited spatial scale but also for efficiency and interaction among genes (Proffitt et al., 2003). The expansion of S. alterniflora patches was mainly due to asexual propagules that extend outward through the maternal roots of the patches. The propagules grow rapidly in the initial stages using nutrients supplied by the maternal roots. Our study revealed that in the early growth stages, the differences between the heights of the offspring propagules and the maternal plants changed with an increase in the height of flooding, and the differences were more pronounced at higher flooding levels (Fig. 4). The phenomenon is due to flooding stress, which affects the supply strategies of roots. In the high flooding area, the seedlings emerging directly from the main roots of the parents grow more rapidly to adapt to external stress. In the upper land boundary, the duration of flooding and the height of flooding were lower; therefore, the epitaxial roots of S. alterniflora could grow rapidly using the nutrients supplied by the maternal plant surpass the maternal plants in the patches. The differences in plant height between the progeny and the maternal plants continued to increase later in the course of growth. Regardless of the heights of the flooding, the propagule heights at the patch edges were higher than in the patch center. The phenomenon of the heights of edge nascent propagules being greater than the heights of maternal plants was also observed in stem diameter (Fig. 5). The new edge seedlings were long and thick, while the interior plants were relatively slender. The phenomenon facilitates the development of patches from new seedlings that break through deeper soils and survive. The differences in stem diameter between the progeny and the maternal plants increased with an increase in flooding height, and the differences in plant height were more uniform. According to the authors, the phenomenon is potentially associated with the senescence of clone centers that have been reported by researchers. In addition, the depletion of nutrients has been suggested as a cause of the death observed in clonal plant centers (Ehrenfeld et al., 2005), and the immobilization of nitrogen in alien invaders could lead to their gradual decline (Christian and Wilson, 1999). Some studies do not support the hypothesis that soil nutrient depletion and plant parasitic nematodes or soil pathogens cause aging. Otfinowski et al. (2007) found the loss of clonal viability and plant parasitic or soil pathogens through patch center aging to be irrelevant in invasive clonal plants in Manitoba, Canada, and the soil in the center of the patches also contained higher soil nitrogen, phosphorus, and moisture (Otfinowski et al., 2007). Such aspects of clonal morphology could vary based on plant genotypes and environmental gradients (e.g., elevation), and clonal variations or densities would also result in habitat heterogeneity (Proffitt et al., 2003). The central senescence of S. alterniflora patches could be a function of age-related ramet mortality (Bell, 1974; Harper, 1977), which is potentially independent of the directional growth of rhizomes. However, Proffitt et al. (2003) do not support the hypotrophy hypothesis because the nutrition structure at the patch center is similar to the nutrition structure at the edge (Egerova et al., 2003). In addition, Carteni et al. (2012), Bonanomi et al. (2014) and other researchers propose the hypothesis that the central death or aging observed by cloned species is caused by accumulated negative plant-soil feedback, which decreases the viability of clonal plants (Carteni et al., 2012; Bonanomi et al., 2014). Such problems remain unaddressed due to the accumulation of soil pathogens over time (Derooijvandergoes, 1995) or rust, which are the potential effects of mutualistic fungus (Mitchell et al., 2002; Rudgers et al., 2005). The nutrient supply strategy of the maternal plant and the adaptive strategy of S. alterniflora against flooding height environments jointly influence the existence of the difference phenomenon. Intraspecific competition between genotypes may produce different results at different elevations. The differences between the edge and interior sections of patches are relatively large and enhanced by nutrients supplement between seedlings and ramets, which lead to considerable spatial heterogeneity.
4.1. Stand characteristics of S. alterniflora with flooding gradient According to the results, the relationship between flooding height and plant heights or stem diameters towards the sea mainly indicated that plant heights at the patch center and of the edge nascent propagules increased with an increase in flooding height (Fig. 4). The stem diameters within the patches also increased with an increase in inundation (Fig. 5). The stem diameters of plants at the patch edges exhibited a unimodal relationship with flooding height in the early growth stages and appeared to increase with an increase in flooding height at the mature stages (Fig. 5). In the patchy distribution area, the expansion of patches was mainly based on the clonal ramets produced by the maternal plants. The populations gradually expanded on the mudflat throughout the invasion period, and the patch distribution area extended its unstable dynamic to the land (Morris et al., 2013). The community and stand characteristics would change during the interannual period and eventually achieve a stable state. Morris et al. (2013) proposed the parabolic law of plants under flooding conditions, which is based on a fundamental concept in ecophysiology referred to as the law of tolerance: if a swamp is on the rising side of a parabolic curve and the submersion is below the optimal level, then production would increase with an increase in sea level, while production in a swamp on the falling part on the right side of the curve would decrease with an increase in sea level (Morris et al., 2002). The productivity hump curve achieves the optimal depth with an increase in inundation, and then production decreases with an increase in depth (Morris et al., 2013). Voss et al. (2013), in field experiments, also observed that two large plants, Spartina and Juncus, showed increased growth with increasing inundation during the growing season. The patchy region in the present study was in an unstable state of development with an increase in inundation levels, and the plant heights and diameters of individuals increased, which demonstrated the positive correlation on the left side of Morris' parabola. Large plants such as S. alterniflora have moderately increased their above-ground growth due to rising sea levels (Kirwan and Guntenspergen, 2012). Therefore, the parabolic relationship between plant growth and submergence could reveal whether the swamp would be stable over an extended period of sea level rise (Voss et al., 2013). The conceptual model of the relationship between tidal submergence and above-ground plant growth is the theoretical basis for the evolution and development of salt marshes, which influences the growth and boundary changes of tidal creek networks and estuarine wetlands, and, in turn, influences species distribution, landscape patterns, and species movements (Moody and Aronson, 2007; Kirwan et al., 2012; Carus et al., 2017). Numerous studies have described the significant correlation between interannual sea level and above-ground biomass and elucidated the close relationship between stand characteristics and sea level (Silinski et al., 2016; Hill and Roberts, 2017; Gittman et al., 2018; Li et al., 2018). The proposed feedback of the parabolic relationship is applicable in relatively stable salt marshes characterized by regular tidal and rich sediments, and a similar relationship is equally applicable in unstable saltmarshes that are undergoing invasion. Alternatively, at low elevations or under rapid rates of sea level rise, increases in inundation decrease vegetation growth and lead to the rapid submergence of marshes. Therefore, a parabolic relationship between plant growth and inundation could potentially explain whether a marsh would be stable for thousands of years or whether it would be submerged rapidly (Morris et al., 2002). 4.2. Advantages of offspring propagules over maternal plants We observed that offspring clonal ramets had some advantages over maternal plants based on stand characteristics between the center and the edges of the patches (Fig. 4 and Fig. 5). This finding is critical not 862
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morphometric quantities and salinity stress in S. alterniflora could be due to increased physiological and anatomical specialization, or could reflect the adaptation of genotypes to other stress factors in addition to salinity (Hester et al., 1998). The elevation relative to the average flooding height is often used as a general indicator of the distribution patterns of species along environmental gradients. In the present study, we use inundation height, a predictable variable that directly influences plant growth, instead of elevation, as a surrogate factor for functionally linked variable effects. Proffitt et al. (2003) reported that seedlings have a wide range of sexual reproduction output, with an average of 24.2 seedlings/m2, with similar rates of emergence in low-elevation areas and high-elevation areas (Proffitt et al., 2003), which was inconsistent with the findings of the present study. In May, during the seedling stage, the seedling emergence rate was low due to the minimal tidal disturbance or high salinity stress at higher elevations. The intervals of survival and adaptation of sexual propagules in the flooding regime is an important reason to determine the population distribution of S. alterniflora. This is an important indicator threshold for evaluating the spreading capacity of the population. Our results confirm that in the extensive estuarine wetlands, the S. alterniflora growth is limited by elevation.
Fig. 6. Heights of sexually (mean ± SE) propagated S. alterniflora seedlings on the bare mudflat. Bars with different letters are significantly different.
4.3. Inundation height adaptation threshold for sexual propagules of S. alterniflora
5. Conclusions
Colonization by sexual propagules has an adaptive flooding height threshold. The emergence rate of seedlings increases with an increase in flooding height and gradually stabilizes at a flooding height of 13–38 cm (Fig. 6), with an average of 3.6–10 seedlings/m2 (Fig. 7). The germination of sexual propagules, seedling supplementation, and subsequent clonal propagation were critical for the expansion of the S. alterniflora populations. Colonization by sexual propagules is a dynamic process that influences the development of patchy areas and is often underestimated. The land boundary in our study area had a high evaporation rate and a relatively low tidal frequency disturbance due to its higher elevation, making salinity higher than in the low elevation area. We conclude that the lower tidal frequency and high salinity or low soil moisture content stress are the major reasons why sexual propagules cannot colonize the higher tide areas of the Yellow River Delta. Although numerous morphological and growth traits are under the influence of genetic control some extent, many are clearly influenced by environmental factors such as elevation (Proffitt et al., 2003). According to Hester et al. (1998), the lack of correlation between
Based on the parabolic relationship between plant productivity and submergent conditions described in Morris et al. (2002), we propose a positive correlation between the above-ground characteristics of S. alterniflora and inundation in an unstable invasive dynamic zone, which is consistent with the correlation suggested for the left side of the parabola in Morris et al. (2002). The interannual variability of tidal inundation conditions would influence the dynamic changes to the boundary of the invasion area. The positive relationship between the stand characteristics and tidal inundation facilitates the gradual expansion of patches that influence tidal networks, interspecific competition, and habitat heterogeneity. To facilitate long-term observations of plant growth and interannual flooding conditions in dynamic invading areas, it is critical to understand the dynamic processes of invasion. It is also important to establish a numerical models for stand characteristics–inundation condition–sedimentary erosion feedback effects on S. alterniflora, which could facilitate the proper assessment and prediction of the impacts of changes in tidal conditions on S. alterniflora invasion linked to sea-level rise, coastal erosion, and human activities.
Fig. 7. The density of sexual (mean + SE) and asexual clone seedlings (mean ± SE) of S. alterniflora. Bars with different letters are significantly different. 863
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Author contributions
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