Biomechanical properties of marsh vegetation in space and time: effects of salinity, inundation and seasonality

Abstract

Background and Aims

Over the last decade, the importance of plant biomechanical properties in shaping wave dissipation efficiency of marsh vegetation has gained growing attention. Here we provide the first analyses of how biomechanical stem properties vary with seasons and along environmental gradients in coastal and estuarine marshes, which is essential to enable accurate assessments of flood defence value of marsh vegetation.

Methods

We quantified both spatial and seasonal variation in stem flexibility and breakability for a variety of common marsh vegetation (Spartina anglica, Scirpus maritimus, Phragmites australis, Elymus athericus, Suaeda maritima, Aster tripolium, Saliconia procumbens) distributed along both salinity and inundation gradients.

Key Results

Increasing salinity tends to induce a shift from species with tall shoots, high flexural stiffness (stem resistance to bending; N mm²) towards species with shorter and more flexible stems. The same trend was found with increasing inundation stress (i.e. decreasing elevation) from the higher part of the low marsh towards the pioneer zone. Stem breakability (the force required to break or fold a stem, N) followed the same pattern of stem stiffness due to the positive relationship between flexural strength (material resistance to flexure, N mm⁻²) and Young’s bending modulus (material resistance to bending; N mm⁻²). Shifts in stem stiffness and breakability at the community level were found to relate positively to the variation in canopy height between species, highlighting the concurrence of changes in morphological and biomechanical traits under environmental changes. Compared to the differences between species, within-species variability between sampling locations and between seasons is generally minor.

Conclusions

Our findings imply that environmental changes may significantly modify wave attenuation capacity of coastal vegetation by inducing species shifts. This emphasizes the need to understand the response of community composition to climate change and human disturbances, when using nature-based flood protection by coastal vegetation as an adaptive response to global change.

Biomechanical properties, wave attenuation, coastal defence, salinity, inundation, season, stem stiffness, stem breakability

Introduction

Increasing flood risks due to climate change and rising sea levels are challenging conventional engineered defences (Temmerman et al., 2013; Bouma et al., 2014; Wahl et al., 2017). This provokes a paradigm shift towards innovative, nature-based solutions by harnessing the coastal defence properties of vegetated coastal ecosystems such as salt marshes (Gedan et al., 2011; Shepard et al., 2011; Temmerman et al., 2013; Bouma et al., 2014). Salt marsh canopies can attenuate waves even under extreme storm conditions (e.g. Moller et al., 2014; Vuik et al., 2016). The capacity for wave attenuation by vegetation depends not only on hydrodynamic conditions such as wave height and water depth (e.g. Ysebaert et al., 2011; Anderson and Smith, 2014; Vuik et al., 2016), but also on properties of the vegetation including standing biomass (e.g. Bouma et al., 2010; Marsooli and Wu, 2014; Vuik et al., 2016) and biomechanical properties such as stem stiffness (e.g. Bouma et al., 2010; Feagin et al., 2011; Lara et al., 2016; Rupprecht et al., 2017) and stem breakability (e.g. Vuik et al., 2018).

Over the last decade, the importance of plant biomechanical properties in shaping wave dissipation efficiency of coastal vegetation has gained increasing attention (e.g. Bouma et al., 2005; Paul et al., 2012; Rupprecht et al., 2015, 2017). Recent studies have shown that plant flexibility plays an important role in determining how salt marsh vegetation interacts with the orbital flows under waves (Rupprecht et al., 2017; Silinski et al., 2018). Plants with different stiffness and flexural strength can differ greatly in their resilience to physical damage under extreme waves (Vuik et al., 2018). Flexible plant species can minimize the risk of folding and breakage through reconfiguration (Bouma et al., 2005; Puijalon et al., 2011). By contrast, stiff plants are more efficient in damping waves by maximizing their resistance to stress (Paul et al., 2016), but may break more easily, resulting in lower wave attenuation capacity (Vuik et al., 2018). Both plant flexibility and resistance to breakage can be expected to be location-specific due to trait differences in species that dominate a habitat along inundation and salinity gradients (Crain et al., 2004, 2008; Pennings et al., 2005). For the same species, these biomechanical properties may differ in space due to changing growing conditions (Silinski et al., 2018) and vary over time because of seasonal cycles of plant growth (Liffen et al., 2011; Miler et al., 2014; Łoboda et al., 2018). However, there is a lack of understanding on how biomechanical properties vary with seasons and along environmental gradients in coastal and estuarine marshes. This knowledge gap hampers accurate assessments of the wave attenuation value of marsh vegetation.

In this study, we quantified spatial and seasonal variation for a range of plant biomechanical characteristics (i.e. flexural stiffness and breaking force of the stem, Young’s bending modulus and flexural strength of the tissue) for a variety of dominant marsh species distributed along both salinity and inundation gradients. Salinity and elevation are known to be key environmental factors that govern both spatial species distribution and plant growth (canopy height, stem diameter, biomass, etc.) in estuarine and coastal marshes (e.g. Pennings et al., 2005; Crain et al., 2008; Ury et al., 2019). Increased salinity stress has been shown to enhance rigidity of leaf tissue (e.g. Touchette et al., 2009, 2014). However, it is still poorly understood how mechanical stem characteristics of marsh plants may vary seasonally and along salinity and inundation gradients. To bridge this knowledge gap, we conducted case studies in six marshes in the Netherlands, where we collected stem samples of plants growing at different elevations and at marshes with different salinity levels. In the lab, we determined stem stiffness and breakability of these samples through three-point bending tests.

MATERIALS AND METHODS

Plant species and sampling sites

We sampled seven common marsh plant species that occur in contrasting environmental conditions (Table 1). To study the effect of salinity, we compared three dominant species that inhabit the lower marsh zone in areas with different salinities: Spartina anglica (Spartina) for salt areas, Scirpus maritimus (Scirpus) for brackish areas and Phragmites australis (Phragmites) for fresh areas. To study the effect of inundation time, we compared species that are characteristic of the different marsh zones along the elevation gradient: Elymus athericus (Elymus) for the high marsh, Suaeda maritima (Suaeda) and Aster tripolium (Aster) for the low marsh, and Saliconia procumbens (Saliconia) for the pioneer zone.

Table 1.

Detailed information on sampling sites (Fig. 1) and time.

Salinity (p.p.t.)	Site	Sampling location	Elevation (m NAP)	Species	Sampling season
0	De Zaag (DZ)	Near marsh edge	0.5	Phragmites australis	Dec 2014, Apr 2015, Jul 2016, Sept 2015
9	Groot Buitenschoor (GB)	Near marsh edge (GBLow)	1.9	Scirpus maritimus	Dec 2014, Apr 2015, Jul 2016, Sept 2015
		25 m from the marsh edge (GBHigh)	2.3	Scirpus maritimus
11	Rilland (RL)	Nearby marsh edge	1.7	Spartina anglica	Dec 2014, Apr 2015, Jul 2016, Sept 2015
		Near marsh edge (RLLow)	1.9	Scirpus maritimus
		50 m to the marsh edge (RLHigh)	2.4	Scirpus maritimus
		100 m to the marsh edge	2.6	Phragmites australis
20	Hellaget Polder (HG)	Near marsh edge (HGLow)	1.0	Spartina anglica	Dec 2014, Apr 2015, Jul 2016, Sept 2015
		50 m to the marsh edge (HGHigh)	1.9	Spartina anglica
24	Zuidgors (ZG)	Near marsh edge	1.9	Spartina anglica	Dec 2014, Apr 2015, Jul 2016, Sept 2015
30	Noord-Friesland Buitendijks (NFB)	Pioneer zone	1.1	Saliconia procumbens	Mar 2016, Jun 2016, Aug 2016, Nov 2016
		Low marsh	1.5	Suaeda maritima
		Low marsh	1.5	Aster tripolium
		High marsh	1.9	Elymus athericus

NAP, refers to Dutch Ordnance Datum which is close to mean sea level.

Fig. 1.

Study sites. Detailed information on sampling time, sampling locations and species types at each site are given in Table 1.

To examine the impacts of salinity, we selected five Dutch marshes with contrasting salinity levels that range from 0 to 30 p.p.t. This included four salt to brackish marshes in the Westerschelde, Groot Buitenschoor (GB), Rilland (RL), Hellaget Polder (HG) and Zuidgors(ZG), and one freshwater marsh De Zaag (DZ) in the river Nieuwe Maas (Fig. 1, Table 1). In these marshes, the three dominant (pioneer) species that we sampled along the salinity gradient were Spartina, Scirpus and Phragmites. Spartina can be found in both salt (ZG) and brackish marshes (RL and HG), while Scirpus is abundant in brackish marshes (RL and GB). Phragmites dominates the fresh water marsh (DZ), but can also be found at higher elevations in the brackish marsh (RL). We sampled all the three species at the brackish site RL, whereas only one species was sampled for the other sites. Where Spartina (HG) or Scirpus (RL) occurred at different elevations within the same marsh, we sampled two locations: one of relatively higher elevation and the other of relatively lower elevation. This was to detect how local elevation differences may influence plant biomechanical properties for the same species (Table 1).

Coastal marshes typically display a zonation of plant species along the elevation gradient, which is also an inundation gradient. Plants growing in the high marsh can differ greatly with those growing in the low marsh (van Loon-Steensma et al., 2016). To investigate how the biomechanical properties may vary between species types along the zonation (elevation) gradient, we conducted a case study in the marsh of Noord-Friesland Buitendijks, located in the Dutch Wadden sea coast (Fig. 1, Table 1), which displays a clear zonation of plant species along the elevation gradient: Elymus in the high marsh, Suaeda and Aster in the low marsh, and Saliconia in the pioneer zone.

For every studied plant species, we sampled four times over the seasonal cycle: spring, summer, autumn and winter (more details see Table 1). Ten stems per species per sampling location were collected on each occasion. At each sampling location, the stems were randomly chosen and cut from the bottom. Once collected, all the samples were taken back to the lab and tested within 48 h to keep the stems as fresh as possible. We also measured canopy height (measured as the distance from the highest point of the plant to the ground) for 30 random individual plants and stem density (determined in five random 50 × 50-cm quadrats) at each sampling location. This was done at the end of the growing season (September–October) when plants reach peak above-ground biomass.

Relevant biomechanical properties

Two groups of parameters can be used to describe the mechanical properties of plants: parameters describing tissue properties versus absolute parameters. Tissue properties are normalized for the dimensions of a tissue, so can be similar, for example, for a thick and a thin stem. They thus describe how tissues differ between species and may adjust to growing conditions. In contrast, absolute parameters integrate tissue properties with tissue dimensions, to describe the tissue properties that belong to a tissue of specific dimensions. The absolute parameters will thus differ between thick and thin stems made from same materials, and can be used to describe when tissue actually fails.

The key normalized parameters to describe the mechanical properties of a plant are (see Table 2 for details on calculation methods):

Table 2.

Details of the methods used to determine biomechanical properties.

Variable	Units	Equation	Description	Reference
Flexural stifness (EI)	N*mm2	EI = (s3F)/(48D)	s is the distance between the two support bars; F/D describes the slope of the linear part of the force–deflection curve. D is the vertical deflection of the stem and F is the corresponding bending force.	Usherwood et al. (1997)
Second moment of area (I)	mm4	I = π (dout4 −din4)/64	dout is the outer diameter and din (if present) is the inner diameter of the stem.	Usherwood et al. (1997)
Young’s bending modulus (E)	N*mm−2	E = EI/I	E is calculated by dividing flexural stiffness (EI) by the second moment of area (I)	Usherwood et al. (1997)
Breaking force (Fmax)	N		Directly recorded by the INSTRON machine
Flexural strength (σmax)	N*mm−2	σmax = s doutFmax/8I	σmax is calculated based on the horizontal span of the stem between the two support bars (s), outer diameter (dout), second moment of area (I) and breaking force (Fmax)	Vuik et al. (2018)

• Young’s bending modulus (E; N mm⁻²) describing how much force has to be applied to bend the material to a given displacement (i.e. a high value of E means lower flexibility of the stem).

• Flexural strength, also called modulus of rupture or bending strength (σ_max; N mm⁻²), which is a measure of the resistance of the material to flexure.

  The key absolute parameters to describe the mechanical properties of a plant are (see Table 2for details on calculation methods):

• Breaking force or maximum bending force (F_max; N), describing the absolute force needed for a stem to break or fold.

• Second moment of area (I; mm⁴) describing the stem morphology, which is calculated based on stem diameter.

• Flexural stiffness (EI; N mm²), which is the product of Young’s bending modulus (E; N mm⁻²) and the second moment of area (I; mm⁴). Flexural stiffness, also called stem flexibility, describes the resistance of a stem against bending (i.e. high values of EI indicate high bending resistance or stiffness, which equals the inverse of flexibility).

Three-point bending tests

We conducted three-point bending tests to determine stem flexibility and flexural strength. This was performed at the lab of the Royal Netherlands Institute for Sea Research (NIOZ) using a universal testing machine (precision ±0.5 %) with a 0.5-kN load cell (Instron 5942, Canton, MA, USA), following the same method as used by Silinski et al. (2018). For each sampling season and sampling location, 10 stems per species were used for bending tests. Stem flexibility and flexural strength were determined for the bottom 5–10 cm of each stem, as this is the section where the stems often break (Vuik et al., 2018). For every stem, we first measured the stem diameter at ~5 cm from the bottom with an electronic caliper (precision ±0.5 mm). For hollow stems, both outer and inner diameters were determined. For Scirpus maritimus, which has solid but triangular stems, the mean length of the three sides of the triangular cross-section multiplied by √3/2 was determined as an equivalent measure of (outer) diameter (Vuik et al., 2018). Span length of the testing section was then determined based on stem thickness (outer diameter), applying a maximum stem diameter/span length ratio of 1: 15 to minimize the shear stress (Usherwood et al., 1997). When the span length was fixed, the stem section for the bending test was then placed centrally onto two support bars and a metal bar was lowered from above at a displacement rate of 10 mm min⁻¹ (Supplementary Data Fig. S1A). The vertical deflection of the stem (D) and the corresponding bending force (F) were recorded (Fig. S1B). Table 2 details how we used these measurements to calculate all absolute and normalized biomechanical properties.

Data analysis

We used two-way ANOVAs to analyse the effects of season and species type on stem thickness and biomechanical properties, i.e. flexural stiffness (EI), Young’s modulus (E), breaking force (F_max) and flexural strength (σ_max). This was first done for the three species along the salinity gradient and later for the four species along the elevation gradient. Post hoc pairwise comparisons were achieved through Tukey honest significant differences (HSD) tests. For each species, we applied Pearson’s correlations to examine the relationships between (1) flexural stiffness and stem thickness, (2) breaking force and stem thickness, and (3) Young’s modulus and flexural strength. Pearson’s correlation was also applied to detect the relationship between biomechanical properties (both flexural stiffness and breaking force of the stem) and canopy height at the community level. Where necessary, the data were square root transformed to improve data normality. All statistical analyses were done in R (https://www.r-project.org), applying a significance level of α = 0.05.

RESULTS

Variation of biomechanical properties along the salinity gradient

There were significant differences of biomechanical properties between the species types along the salinity gradient (Table 3). Increasing salinity was found to induce a shift from species with stiff stems towards more flexible stems (Fig. 2A). As expected, flexural stiffness (EI; N mm²) increased positively with stem thickness and Young’s modulus (E; N mm⁻²), i.e. with flexibility of the tissue (Fig. 2A). Due to a higher Young’s modulus, Phragmites, which dominates in freshwater and brackish habitats, had much stiffer stems than the brackish species Scirpus (Fig. 2A). With shorter stems and lower Young’s modulus than the other two species, the salt-tolerant species Spartina had the lowest stem stiffness among the three species (Fig. 2A). Similar to results for flexural stiffness, breaking force (F_max; N) also showed a decreasing trend for the three species along the salinity gradient (Fig. 2B), which can be explained by the positive relationship between flexural strength (σ_max; N mm⁻²) and Young’s bending modulus of the tissue (Fig. 2C).

Table 3.

ANOVA table of the effects of species type and season on biomechanical properties and stem thickness of the three sampled species along the salinity gradient.

Response variable	Source	d.f.	F value	Pr(>F)
	Species	2	169.320	<0.001
Flexural stiffness	Month	3	0.747	0.525
	Species:Month	6	4.135	<0.001
	Species	2	346.106	<0.001
Breaking force	Month	3	21.706	<0.001
	Species:Month	6	8.246	<0.001
	Species	2	48.957	<0.001
Young’s modulus	Month	3	3.641	0.013
	Species:Month	6	4.290	<0.001
	Species	2	115.670	<0.001
Flexural strength	Month	3	1.443	0.230
	Species:Month	6	17.801	<0.001
	Species	2	460.809	<0.001
Stem thickness	Month	3	14.305	<0.001
	Species:Month	6	10.438	<0.001

Fig. 2.

Pearson’s correlations between (A) flexural stiffness and stem thickness, (B) breaking force and stem thickness, and (C) flexural strength and Young’s modulus for Phragmites, Scirpus and Spartina, respectively. The values of flexural stiffness, breaking force and Young’s modulus were square root transformed to improve linearity.

Variation of biomechanical properties along the elevation gradient

Our case study in the marsh NFB showed that biomechanical properties can vary drastically with changing species along the inundation gradient (Table 4). With species shifts along the elevation gradient, stem stiffness and stem breakability first increased and then decreased. The high marsh was dominated by the thin and flexible species Elymus, whereas the vegetation then shifted from thicker and stiffer species (i.e. Aster and Suaeda) in the higher low marsh towards the thinner and more flexible species Saliconia in the pioneer zone (Fig. 3). Whereas flexural stiffness of the two stiffer species Aster and Suaeda showed a clear increasing trend with growing stem thickness, the two more flexible species Elymus and Saliconia displayed no such trend (Fig. 3A). Breaking force of the four species (Fig. 3B) followed the same pattern of stem stiffness due to the positive relationship between flexural strength and Young’s bending modulus of the tissue (Fig. 3C).

Table 4.

ANOVA table of the effects of sampling site and season on flexural stiffness and breaking force for the stems of the three sampled species along the salinity gradient

Species	Response variable	Source	d.f.	F value	Pr(>F)
Phragmites	Flexural stiffness	Site	1	18.843	<0.001
		Month	3	13.766	<0.001
		Site:Month	3	4.738	0.005
Phragmites	Breaking force	Site	1	1.760	0.189
		Month	3	13.499	<0.001
		Site:Month	3	7.165	<0.001
Scirpus	Flexural stiffness	Site	3	8.561	<0.001
		Month	3	6.769	<0.001
		Site:Month	9	3.781	<0.001
Scirpus	Breaking force	Site	3	1.982	0.119
		Month	3	23.822	<0.001
		Site:Month	9	5.028	<0.001
Spartina	Flexural stiffness	Site	3	3.607	0.015
		Month	3	0.441	0.724
		Site:Month	9	2.671	0.007
Spartina	Breaking force	Site	3	33.9781	<0.001
		Month	3	13.7365	<0.001
		Site:Month	9	6.6817	<0.001

Fig. 3.

Pearson’s correlations between (A) flexural stiffness and stem thickness, (B) breaking force and stem thickness, and (C) flexural strength and Young’s modulus for Elymus, Aster, Suaeda and Saliconia, respectively. The values of flexural stiffness, breaking force and Young’s modulus were square root transformed to improve linearity.

General trends

Across-species analysis showed that shifts in absolute values of stem stiffness and breaking force at the community level were related positively to the variation in canopy height between species (Fig. 4). The tallest species Phragmites had the highest flexural strength and breaking force. The two taller low marsh plants, Aster and Suaeda, had higher stem stiffness and breaking force than the two shorter species Spartina and Saliconia that dominate the pioneer zone of saline wetlands (Fig. 4). For all the sampled species, there were significant differences between seasons in biomechanical stem properties (Tables 4 and 5). However, the seasonal variability was species-specific and location-specific without any common trends (Figs 5–7). For instance, there was a significant decline in flexural strength for Scirpus and Phragmites from autumn (September–October) to winter (December) when plants turn brown, whereas the opposite was found for Spartina (Fig. 6B). For the same species, there were also significant differences (Table 4) in stem stiffness (Fig. 5) and stem breakability (Fig. 6) between sampling locations. Within-species variations between seasons and between sampling locations, however, were generally minor compared to the differences between species (Figs 5–7).

Table 5.

ANOVA table of the effects of species type and season on biomechanical properties and stem thickness of the four sampled species along the inundation gradient

Response variable	Source	d.f.	F value	Pr(>F)
	Species	3	30.767	<0.001
Flexural stiffness	Month	3	114.612	<0.001
	Species:Month	9	7.237	<0.001
	Species	3	44.114	<0.001
Breaking force	Month	3	74.767	<0.001
	Species:Month	9	11.893	<0.001
	Species	3	8.614	<0.001
Young’s modulus	Month	3	152.638	<0.001
	Species:Month	9	6.732	<0.001
	Species	3	61.385	<0.001
Flexural strength	Month	3	90.673	<0.001
	Species:Month	9	12.490	<0.001
	Species	3	145.545	<0.001
Stem thickness	Month	3	6.501	<0.001
	Species:Month	9	6.927	<0.001

Fig. 4.

Across all the sampled species in this study, there were significant positive relationships (Pearson’s correlation) between mean flexural stiffness and mean peak canopy height (A), as well as mean breaking force and mean peak canopy height (B). Prior to the analysis, the values of mean flexural stiffness and mean breaking force were square root transformed to improve linearity.

Fig. 5.

Seasonal changes (mean ± s.e.) of flexural stiffness (A) and Young’s modulus (B) of Phragmites, Scirpus and Spartina at different sampling sites. Different letters indicate significant differences (P < 0.05, Tukey’s HSD test). Inundation ratio refers to the averaged percentage of inundation time per day.

Fig. 6.

Seasonal changes (mean ± s.e.) of breaking force (A) and flexural strength (B) of Phragmites, Scirpus and Spartina at different sampling sites. Different letters indicate significant differences (P < 0.05, Tukey’s HSD test). Inundation ratio refers to the averaged percentage of inundation time per day.

Fig. 7.

Seasonal changes (mean ± s.e.) in stem thickness (A) and biomechanical properties (B–E) of Elymus, Aster, Suaeda and Saliconia along the elevation gradient. Different letters indicate significant differences (P < 0.05, Tukey’s HSD test).

Discussion

A number of studies have assessed the biomechanical stem properties of specific marsh species, including Atriplex (Halimione) portulacoides (Feagin et al., 2011), Scirpus spp. (Coops and Van der Velde, 1996; Heuner et al., 2015; Carus et al., 2016; Silinski et al., 2018; Vuik et al., 2018), Spartina spp. (Feagin et al., 2011; Rupprecht et al., 2015; Lara et al., 2016; Vuik et al., 2018), Phragmitis australis (Coops and Van der Velde, 1996), Elymus athericus (Moller et al., 2014; Rupprecht et al., 2015) and Puccinellia maritima (Moller et al., 2014; Rupprecht et al., 2015; Lara et al., 2016). This study for the first time provides analyses on the spatial (i.e. along salinity and inundation gradients) and temporal (i.e. seasonal) variations in biomechanical stem properties of marsh vegetation. Our case studies in Dutch marshes on the seven dominant species clearly demonstrate that variation in plant morphology (stem thickness) and material properties (i.e. Young’s modulus and flexural strength) between species can cause large differences in the absolute values for stem stiffness and breakability along environmental gradients and over seasons. Given the critical role of these biomechanical properties in determining wave attenuation efficiency of coastal vegetation (Bouma et al., 2005; Paul et al., 2012; Rupprecht et al., 2015, 2017), such spatial and temporal variation may induce considerable variation in the wave attenuation capacity of marsh vegetation, which should be taken into account when modelling the biogeomorphic development or efficiency of nature-based flood defences with marsh vegetation.

Effects of phenotypic plasticity vs. shifts in species

Studies have shown that both terrestrial and aquatic plants display plasticity in biomechanical properties as adaptive responses to changing environmental stresses (Read and Stokes, 2006; Carmen et al., 2016; Silinski et al., 2018). A recent study on a single marsh plant, Scirpus maritimus, found that stems become more flexible with increasing wave stress (Silinski et al., 2018). The current study on multiple species along the salinity gradient and inundation gradient demonstrate that variation of biomechanical properties as a response to changing stress levels can even be bigger when inducing changes at the community level. Our results reveal that raised salinity levels in the low marsh can induce a shift from stiffer species such as Phragmites towards more flexible species such as the brackish marsh pioneer Scirpus and the salt-water pioneer Spartina (Fig. 2). Increased inundation may cause a shift in the low marsh from stiffer plants such as Aster to the more flexible species Saliconia or Spartina (Figs 3 and 4). This means that species shifts resulting from environmental changes such as salt water intrusion and alteration of freshwater discharge (Neubauer and Craft, 2009) may cause considerable changes in plant biomechanical properties and thus wave attenuation values.

Shoot length as a key driver of species differences in biomechanics

The current study highlights in particular that variation in biomechanical properties at the community level is closely related to differences in plant canopy height between species. Taller species tend to have stiffer and stronger stems than shorter ones (Fig. 4), which may result from the fact that taller plants generally need stronger shoots to support the higher biomass (Jagels et al., 2018). A positive relationship between plant morphology and biomechanical properties has been similarly seen in other plant communities. A comprehensive analysis of the mechanical and morphological traits of seagrasses showed that larger leaves typically had higher leaf breaking force, to tolerate the greater drag forces due to the larger leaf area (Carmen et al., 2016). The positive link between stem biomechanical properties and canopy height could explain the variation in stem stiffness and breakability along salinity and inundation gradients. Increased salinity and inundation can induce a change of vegetation from taller plants towards shorter ones. As a consequence, plant stems shift from being stiffer and stronger towards being more flexible and weaker. In addition, while taller species tend to have higher thresholds for stem breakage, they may still break more easily than shorter ones due to the higher contact area with water (Vuik et al., 2018).

Species-specific differences in seasonality may explain differences in stem breakage

Seasonality is a key environmental factor that governs plant functional traits such as canopy height (e.g. Liu et al., 2004), stem diameter (e.g. this study, Singh et al., 1990) and shoot density (e.g. Orth and Moore, 1986), yet its effects on plant biomechanical properties are generally overlooked in previous studies (but see Łoboda et al., 2018). In this study, all examined species show seasonal variability in biomechanical properties, while the variation trend is species-specific. For instance, flexural strength of Spartina was highest in winter (December), whereas it was lowest for Scirpus in the same season (Fig. 6B). Such difference may explain the observed difference in stem breakage between these two species. Spartina can preserve most of its above-ground biomass until the end of winter, whereas most Scirpus stems break from autumn onwards (Vuik et al., 2018). Information on seasonal variation in stem breakability is essential to enable accurate assessments of the flood protection value of coastal vegetation, as the timing of storms varies with geographical locations, and coinciding seasonal variations in storm intensity and vegetation characteristics determine to what extent vegetation may contribute to flood protection during storms (Moller et al., 2014; Vuik et al., 2016, 2018).

Effect of global change on the biomechanics of marsh vegetation

For the same species, biomechanical properties can differ between sampling locations as a response to variations in growing conditions such as salinity level and water depth. Yet such differences are negligible compared to the differences between species. These results suggest that environmental changes such as increased inundation period due to sea level rise or enhanced salinity because of salt intrusion would not result in major changes in plant biomechanical properties, unless they induce shifts in species. In addition to biomechanical properties, shifts in species also alter other properties in relation to wave attenuation such as stem density (Table 6), canopy height (Fig. 4, Table 6) and stem thickness (Figs 2 and 3). For instance, increased drought has shifted the dominant vegetation type in a Mediterranean salt marsh from the tall, dense and stiff Spartina to the short, sparse and more flexible Saliconia (Strain et al., 2017). The changes in plant morphological traits and biomechanical properties will inevitably result in significant changes in wave attenuation values of the salt marsh (Bouma et al., 2005, 2014; Ysebaert et al., 2011; Vuik et al., 2016).

Table 6.

Stem density (mean ± s.d.) and canopy height (mean ± s.d.) of all the sampled species at the end of the growing season (September–October)

Species	Stem density (no. m–2)	Sample size	Canopy height (cm)	Sample size
Phragmites	309 ± 103	10	236 ± 62	60
Scirpus	352 ± 75	20	103 ± 25	120
Spartina	1092 ± 269	20	51 ± 13	120
Saliconia	520 ± 49	5	25 ± 6	30
Suaeda	201 ± 69	5	62 ± 8	30
Aster	67 ± 38	5	110 ± 30	30
Elymus	1098 ± 143	5	36 ± 9	30

Implications for modelling wave attenuation by coastal vegetation

The presented seasonal and species-specific data on stem bending strength (σ_max) can feed the stem breakage model that predicts storm wave-induced vegetation loss, based on physical conditions and vegetation properties including σ_max (Vuik et al., 2018). This is crucial for enabling accurate calculation of wave attenuation during extreme conditions that remove weak plants (e.g. Moller et al., 2014; Rupprecht et al., 2017; Vuik et al., 2018). Another essential input for calculating wave dissipation by coastal vegetation is bulk drag coefficient (Mendez and Losada, 2004), which is largely determined by stem flexibility (e.g. Bouma et al., 2010; Vuik et al., 2016; Rupprecht et al., 2017). Yet, bulk drag coefficient (C_D) is determined usually by calibration of this parameter with respect to the Reynolds number (Re), based on experiments (Mendez and Losada, 2004; Moller et al., 2014; Vuik et al., 2016). Here, we advocate that data on stem flexibility (EI) of different species and seasons should be combined with measurements of flow regime and wave dissipation, to explore the possibility of establishing quantitative relationships between EI and C_D. Once such relationships are established, one can derive C_D of a certain species for a given season based on the corresponding EI. This would mean models for computing wave attenuation by different vegetation type at different seasons could be applied without experimental calibration of drag against observed dissipation.

Conclusions

Overall, the current study highlights the importance of season and environmental gradients in determining the biomechanical properties of coastal vegetation, which are key determinants for its wave attenuation capacity and thus its value as nature-based coastal defence. While previous studies underline the role of variability in plant mechanical traits as adaptation strategies to biotic (e.g. herbivory: Lucas et al., 2000; Sanson et al., 2001) and abiotic mechanical forces, such as wind (Cordero, 1999; Pigliucci, 2002) or hydrodynamics (Bouma et al., 2005; Puijalon et al., 2011; Silinski et al., 2018), our study indicates that shifted biomechanical properties as a result of self-adaptation to changed environmental conditions can have cascading effects on the role of plants in climate adaptation. Detailed information on the biomechanical properties of the seven common salt marsh vegetation types can provide useful inputs for numerical models that seek to assess the spatial and temporal variation of wave attenuation by coastal vegetation, which is a vital but often ignored step in the design and implementation of nature-based flood protection. Our findings also suggest that climate change may cause major changes in coastal protection functions of salt marshes by inducing shifts in dominant species types, imposing long-term uncertainties over nature-based flood protection.

SUPPLEMENTARY DATA

Supplementary data are available online at https://academic.oup.com/aob and consist of the following. Fig. S1: (A) Set-up of the Instron three-point bending test; (B) a typical force–displacement curve.

FUNDING

This work is part of the research programme BESAFE, which is financed by the Netherlands Organization for Scientific Research (NWO). Additional financial support was provided by Deltares, Boskalis, Van Oord, Rijkswaterstaat, World Wildlife Fund, HZ University of Applied Science.

ACKNOWLEDGEMENTS

We thank Isabella Kratzer, Vincent Vuik, Li Ma and Yifei Gu for their help in collecting samples and in the lab tests. We are also grateful for the assistance received from Peter Esselink, Georgette Lagendijk and It Fryske Gea during our field campaigns in the marsh of Noord-Friesland Buitendijks. The biomechanical property data from this study are available from the Figshare Digital Repository (https://doi.org/10.6084/m9.figshare.7881062.v1).