Ecological Engineering 61 (2013) 12–22
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Ecological Engineering
j ournal homepage: www.elsevier.com/locate/ecoleng
Mineral versus organic contribution to vertical accretion and
elevation change in restored marshes (Ebro Delta, Spain)
a,∗ b b c a
Juan Calvo-Cubero , Carles Ibánez˜ , Albert Rovira , Peter J. Sharpe , Enrique Reyes
a
Department of Biology, East Carolina University, Greenville, NC, USA
b
Aquatic Ecosystems Program, IRTA. St. Carles de la Ràpita, Catalonia, Spain
c
US National Park Service, 120 Chatham Lane, Fredricksburg, VA 22405, USA
a r t i c l e i n f o a b s t r a c t
Article history: The Ebro Delta (Catalonia, Spain) is one of the most valuable coastal zones within the Mediterranean
Received 2 May 2013
Sea, supporting a highly productive rice agricultural system, as well as a myriad of coastal marsh habi-
Received in revised form 9 August 2013
tats. However, chronic reductions of fluvial sediments coupled with accelerated relative sea-level rise
Accepted 20 September 2013
have created an environment where approximately half of the Ebro Delta is now vulnerable to flood-
ing impacts. To assess relative sea-level rise (RSLR) mitigation options through marsh restoration within
Keywords:
abandoned deltaic rice fields, we established the experimentally restored marshes spanning three years.
Sea-level rise
We used two freshwater input type treatments (riverine irrigation and rice field drainage water) and
Marsh restoration
three water level treatments (10, 20 and 30 cm deep). Our hypotheses were that: (1) vertical accretion
Root growth
and elevation change in oligohaline restored marshes would be primarily controlled by organic contrib-
Marsh elevation
Sediment inputs utions under sediment-deficit conditions, and (2) both vertical accretion and elevation change would
−1
Paspalum distichum demonstrate higher rates compared with predicted RSLR in the Ebro Delta (5–8 mm yr ). Vertical accre-
−1
tion had higher mean values in both water type treatments (11.5 and 15.5 mm yr ) than elevation change
−1
(9.1 and 8.8 mm yr ). Vertical accretion (but not elevation change) was significantly higher in drainage
water treatment receiving greater sediment mineral input, which caused higher surface soil mineral con-
tent. Conversely, experimentally restored marshes closer to rice fields in both water type treatments had
−1 −1
greater elevation change (11.3 and 17.8 mm yr ) than vertical accretion (8.3 and 15.1 mm yr ) due to
higher belowground biomass because of high weed colonization by Paspalum distichum L. These results
showed that vertical accretion and elevation change were generally controlled by mineral contribution,
although fast growing, ruderal plant species such as P. distichum can play a significant role in marsh ele-
vation via root growth. The results supported the hypothesis that restored marshes using either water
type promote marsh elevation gains higher than predicted RSLR at least during the initial marsh devel-
opment (3 years). This study indicates that the use of agricultural runoff as a primary source of sediment,
nutrient, and freshwater is beneficial for marsh restoration projects focused primarily on mitigating RSLR.
This research also highlights how nuisance species such as P. distichum can play a key role in mitigating
RSLR impacts when inexpensive and effective measures are needed to promote marsh elevation as the
primary restoration goal.
Published by Elsevier B.V.
1. Introduction the Natura 2000 network of the European Union (EU). Jux-
taposed with these natural areas there are 20,000 Ha of rice
The Ebro Delta is a vital coastal ecosystem in the western fields. Rice agriculture is the main economic activity within the
2
Mediterranean extending ∼330 km (Fig. 1) and is the second Delta comprising up to 60% of the land surface of the Ebro
most important special protection area for birds (SPA) in Spain Delta, providing an annual gross income of about D 60 million
(Seo/BirdLife, 1997). The Ebro Delta possesses a diverse number and a total rice production of 120,000 tons per year (Cardoch
of ecosystems including coastal lagoons, marshes and seagrasses, et al., 2002). Although rice agriculture development has trans-
which comprise the Ebro Delta Natural Park and are part of formed much of the Ebro Delta over the last two centuries
(Cardoch et al., 2002), rice fields provide significant ecosystem
services such as seasonal habitat for migratory birds, preven-
∗ tion of saline intrusion and nutrient removal (Martinez-Vilalta,
Corresponding author. Tel.: +1 252 328 5778.
E-mail address: [email protected] (J. Calvo-Cubero). 1995).
0925-8574/$ – see front matter. Published by Elsevier B.V. http://dx.doi.org/10.1016/j.ecoleng.2013.09.047
J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22 13
the global market by reduced production and subsequent increases
in rice prices, which may have important implications for food
security (Chen et al., 2012). Several studies in the Mediterranean
and Asian Deltas (e.g. Ebro, Nile, Ganges and Mekong Deltas) also
suggest potential population displacements, loss of biodiversity
and cultural heritage (Syvitski et al., 2009; Day et al., 2011).
One proposed measure to mitigate deltaic impacts is the intro-
duction of riverine sediments into marshes as a means of correcting
the sediment deficit (e.g. Mississippi Delta, Rhone Delta and Ebro
Delta) (Ibánez˜ et al., 1997; DeLaune et al., 2003; Day et al., 2007).
The reintroduced river water would also provide a source of nutri-
ent input, which theoretically would increase marsh elevation
by stimulating autogenic organic contribution via plant growth
(McKee and Mendelssohn, 1989; Day et al., 2008). Freshwater
inputs also reduce soil stressors such as hyper-salinity, anoxia
and toxins that typically inhibit plant growth (Day et al., 2011).
Several studies also emphasize that the organic contributions to
marsh elevation may be more relevant than mineral contributions
in sediment-deficient deltas and estuaries (DeLaune and Pezeshki,
2003; Blum and Christian, 2004; Nyman et al., 2006). However,
more data are required to directly link organic contribution to
marsh elevation (Cahoon et al., 2006; Day et al., 2011; Fagherazzi
et al., 2012). In the Ebro Delta only marshes that maintain signifi-
cant freshwater and sediment inputs will likely survive predicted
RSLR (Ibánez˜ et al., 2010). So it is important to understand under
which conditions the mineral and organic contributions to marsh
elevation can be optimized as a key restoration objective. For exam-
ple, the use of Paspalum Distichum L. during the establishment of
restored marshes may be a viable restoration practice to mitigate
RSLR due its ability to capture sediments, it’s tolerances to salinity,
water logging, and dry conditions, fast growth, and ability to repro-
duce from rhizomes, stolons, or seeds (Anderson and Ehringer,
2000; Carr, 2010; Wanyama et al., 2012). The practice of converting
rice fields into marshes in areas of low elevation has been proposed
in the Ebro Delta as a way to mitigate the effects of climate change
(e.g. by elevation gain and carbon sequestration) and improve the
water quality of agricultural runoff (Ibánez˜ et al., 1997). Recently,
several public efforts have restored rice field land to freshwater
Fig. 1. The top map shows the location of the experimentally restored marshes marshes in the Ebro Delta using river irrigation water or rice field
in the Ebro Delta (Catalonia, Spain). The bottom map shows its detailed location
drainage water to feed them (MARM, 2006; Ibánez˜ and Bertolero,
between an active organic rice field and an old restored marsh dominated by Phrag-
2009). However, no previous experimental studies in the Ebro
mites australis (Cav.) Steudel and Typha latifolia L.
Delta and other Mediterranean deltas have assessed restoration
initiatives regarding abiotic and biotic factors controlling vertical
The marshes and rice fields within the Delta receive irrigation accretion and elevation change to keep pace with sediment deficit
water from the Ebro River, which is the largest river of the Iberian and RSLR.
3 −1
∼
Peninsula (flow ca. 400 m s ). A series of dams ( 170) were In this study we hypothesized that: (1) vertical accretion
built along the watercourse during the 1960s to support a vari- and elevation change in oligohaline restored marshes under low
ety of intensive water uses (Ibánez˜ and Prat, 2003). These dams sediment availability conditions are controlled by organic con-
retain an estimated 99% of the sediment that would normally be tributions as a function of water type and water level, and (2)
deposited within the Ebro Delta, thus creating a severe sediment oligohaline restored marshes can have rates of vertical accre-
deficit (Ibánez˜ et al., 1996). Global eustatic sea-level rise (ESLR) has tion and elevation gain higher than RSLR under low sediment
−1
increased at a rate of 1–2 mm yr over the last century and it is availability conditions. To test these hypotheses, we conducted
−1
now higher than 3 mm yr (FitzGerald et al., 2008). However, pre- an experimental study during three years in a newly established
dicted relative sea-level rise (RSLR) in Ebro Delta may range from 5 experimentally restored marshes consisting of 72 experimental
−1 2
to 8 mm yr at the end of the present century, due to ESLR and land units (100 m each). Two different freshwater water input types
subsidence (Ibánez˜ et al., 2010). Both sediment reduction and RSLR (riverine irrigation water and rice field drainage water) and three
∼
have created an environment where 40% of the emerged Ebro water levels (10, 20 and 30 cm deep) were used.
Delta plain has an elevation lower than 50 cm and ∼10% of the delta
is below sea level (Ibánez˜ et al., 1997). Thus, 50% of the Ebro Delta
is vulnerable to flooding impacts and permanent submergence of 2. Methods
both marshes and rice fields (DMAiH, 2008; Alvarado-Aguilar et al.,
2012). This is not a problem unique to the Ebro Delta as similar 2.1. Experimental design
systems such as the Ganges, Mississippi, Nile, Rhone and Po Deltas,
all suffer from similar sediment deficits (Syvitski et al., 2009). RSLR We carried out the field experiment at an organic rice farm
impacts on worldwide deltaic rice agriculture would have effects on located in the southeast of the Ebro Delta (Catalonia, Spain) (Fig. 1,
14 J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22
Fig. 2. Design of the experimentally restored marshes. The two water treatments consisted of 36 experimental units receiving either irrigation or drainage water. Each
treatment included the water level factor (10, 20 and 30 cm depth) divided in 3 blocks via a complete randomized block design.
top). We established the experiment between an active organic Phragmites australis (Cav.) Steudel, Scirpus maritimus L. and Scirpus
rice field to the West and an old restored marsh to the East sep- litoralis Schrad., since the study area is located in an old freshwater
arated by a bare soil strip (Fig. 1, bottom). We used a partly nested marsh area (abandoned distributary), which was transformed to
experimental design to compare plant biomass, vertical accre- rice cultivation in the previous century (Curcó et al., 1995).
tion and elevation change in response to water type and water We initiated the experiment in August 2009 and ran it for 3 years
level treatments. Water type comprised 2 treatments: riverine (Appendix 1). The hydroperiod for the experiment (seasonal flood-
irrigation water (IW) and rice field drainage water (DW) applied ing and draw down periods) was coincident with the regional rice
to 36 experimental units (EUs) for each treatment. The water level harvest/planting regime. During the first year, the EUs were fully
factor consisted of 3 water level treatments of 10, 20, and 30 cm flooded from August to December. In the second and third years,
in depth. These water level treatments were applied inside each the EUs were flooded from June to December. Targeted water levels
−1
water type using a complete randomized block design with three were maintained using an average water in-flow rate of 4.5 L s .
blocks. Therefore, each water type included 3 blocks and where The EUs were individually isolated using plastic lined wooden walls
each block included 12 EUs; 4 replicate EUs for each three water to prevent/limit water loss.
levels (Fig. 2). We included a block design to account for the varia-
tion in our experimental units from plant colonization effects from 2.2. Water and soil analysis
the active rice field on the West side of the experiment. The cho-
sen water types and levels were based on readily available water Physical and chemical parameters were analyzed monthly from
sources and a realistic range of potential water levels found in rice 2009 to 2011 for both water type inflows (3 samples per month
fields and marshes of the Ebro Delta. Freshwater from both IW and and water type). Dissolved oxygen (DO2), temperature, conduc-
DW favors the development of a helophytic marsh dominated by a tivity and pH were measured using an YSI 556 multiprobe (YSI
J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22 15
Table 1
Incorporated, Yellow Springs, OH, USA). Three water samples per
Mean and standard error of water characteristics of both water type inflows. An
month were collected for both water type inflows during 2010
asterisk indicates a significance difference (˛ = 0.05) on repeated measures ANOVA
and 2011 to measure total suspended solids (TSS), and total inor- −
results between water type inflows for water nutrient content (TP, P-PO4 , TN, N-
− +
ganic suspended solids (TISS) according to the UNE-EN 872 norm NO3 and N-NH4 ) and sediment inputs (TSS and TISS).
(AENOR, 1996). TSS and TISS analysis quantifies both total and
Parameter Water type inflows
mineral sediment inputs in both water types that may cause ver-
Irrigation water Drainage water
tical accretion and elevation change response. In addition, three
◦
water samples per month for both water type inflows during 2010 Temperature ( C) 20.67 ± 1.74 20.56 ± 2.72
± ±
were analyzed for the following nutrients: total phosphorus (TP) pH 8.59 0.20 7.73 0.25
−1
DO2 (mg L ) 7.75 ± 0.94 5.55 ± 0.75
and total nitrogen (TN); inorganic dissolved nutrients; phosphate
−1
± ±
3− − + Conductivity (mS cm ) 1.22 0.10 1.48 0.18
(P-PO4 ), nitrate (N-NO3 ) and ammonium (N-NH4 ), following −1
TP (mg L ) 0.08 ± 0.01 0.18 ± 0.02*
− −
standard methods (Grasshoff et al., 1999). Water nutrient analy- 1
P-PO4 (mg L ) 0.10 ± 0.04 0.13 ± 0.04
−1
± ± sis quantifies nutrient inputs in both water types that may cause a TN (mg L ) 1.18 0.04 1.05 0.21
− −1
± ±
N-NO (mg L ) 1.40 0.17* 0.54 0.13 plant growth response. 3
+ −1
N-NH4 (mg L ) 0.05 ± 0.01 0.22 ± 0.09*
Furthermore, the same physical and chemical parameters were −1
TSS (mg L ) 4.38 ± 0.67 26.66 ± 3.83*
analyzed from a subset of 26 randomly selected EUs (Fig. 2) from the −1
±
±
TISS (mg L ) 2.49 0.51 23.16 3.36*
surface and sub-soil (0.5 m depth) from 2009 to 2011 to monitoring
water characteristics that may influence plant growth. Superfi-
cial soil core samples (above marker horizons) were collected sampled at the end of the experiment (May 2012). SET stations
in May 2011 within a 36 EUs subset to analyze soil parameters were established adjacent to the marker horizons in 26 randomly
(i.e. mineral matter content, bulk density and mineral particle selected EUs (Fig. 2) and SETs readings were taken every three
size) that may impact vertical accretion. Samples of known vol- months since August 2009 until May 2012. In this study we use ver-
ume were weighted to determine wet weight and dried to a tical accretion to refer to surface accretion processes due to mineral
◦
constant weight at 60 C. Soil bulk density was calculated from sedimentation, leaf litter deposition and root growth. We refer to
these data (Page et al., 1982). Organic matter content was mea- elevation change as the change of marsh elevation due to vertical
◦
sured by loss-on-ignition at 500 C during 12 h and mineral matter accretion, subsurface soil expansion by root growth and shallow
was derived from organic matter percentage following Pont et al. subsidence by compaction and decomposition.
(2002). The determination of particle size distribution in mineral
soil material was performed using wet sieving and sedimenta- 2.5. Statistical analysis
tion technique (ISO11277, 2002). The following particles sizes
classes were measured: clay (d < 2 m), fine silt (2 m < d < 16 m), A repeated measures analysis of variance (ANOVA) of fixed
medium silt (16 m < d < 45 m), coarse silt (45 m < d < 63 m) effects (Type III test) was performed to test differences in sedi-
and sand (63 m < d < 2000 m). ment input (TSS and TOSS) and nutrient content (total nutrients and
dissolved inorganic nutrients) on both water type inflows, which
2.3. Aboveground and belowground plant biomass may cause a different response of vertical accretion and elevation
change in the experimentally restored marshes. Multivariate Prin-
Maximum aboveground biomass (MAB) or peak standing crop cipal Component Analysis (PCA) was carried out to explore the
was measured to obtain an estimate of plant growth (Cronk and relationships between abiotic and biotic variables with vertical
Siobhan Fennessy, 2001) that may affect vertical accretion and ele- accretion and elevation change and identify underlying factors that
2
vation change. Accordingly, three random subsamples of 0.25 m control them. Kaiser–Meyer–Olkin’s (KMO) measure of sampling
were sampled from the previously identified 36 EUs subset in the and Barlett’s test of sphericity were used to assess the appropri-
last growing season of the experiment (August 2011) following ateness and adequacy of the PCA (McGarigal et al., 2000). A partly
a direct method from Schubauer and Hopkinson (1984). Plants nested ANOVA of fixed effects (Type III test) was used to test differ-
◦
were separated by species and dried to constant weight (at 60 C). ences on the main response variables (plant biomass, surface soil
Maximum belowground biomass (MBB) was analyzed to obtain properties, vertical accretion and elevation change) among water
information of root growth contribution to vertical accretion and types and water levels (Quinn and Keough, 2002). Differences in
elevation change. MBB was sampled in the last dormant season of response variables among block effects were also analyzed to test
the experiment (May 2012) by collecting two soil core subsamples vertical accretion and elevation change response to vegetation col-
˛
from the 36 EUs subset (50 cm long, 11.8 cm internal diameter). onization. In the presence of significant differences ( < 0.05) in
To improve the efficiency of core extraction, we sealed the top ANOVA results, pairwise comparisons were made with the Tukey
with a screw top cap before extracting the core from the sed- test. All statistical analyses were performed using SPSS software
iment (Schurman and Goedewaagen, 1971). Each soil core was version 20 (IBM, 2010).
sectioned and washed with tap water through 1 mm mesh sieve to
remove inorganic sediments. The plant material was then sealed 3. Results
◦
into labeled plastic bags and stored at 2–5 C. Each thawed sam-
ple was sorted into live and dead roots and litter. All samples were 3.1. Water characteristics
◦
dried to constant mass at 60 C and weighed (Curcó et al., 2002).
Both water type inflows were characterized as oligohaline
2.4. Vertical accretion and elevation change and oxygenated waters (Table 1). The ANOVA indicated DW
inflow had significantly higher TSS (F1,4 = 59,247, P < 0.001), TISS
+
Vertical accretion and elevation change were determined using (F1,4 = 58,285, P < 0.001), N-NH4 (F1,4 = 73.8, P = 0.001) and TP
marker horizons (Kaolinite) (Cahoon and Turner, 1989) and surface (F1,4 = 29.81, P = 0.05) compared to IW (Table 1). IW inflow had
−
elevation tables (SETs), respectively (Cahoon et al., 2002). Marker significantly higher N-NO3 (F1,4 = 51.67, P = 0.002) with no signifi-
2 3−
horizons were laid upon a 1 m marsh surface in the center of the cant differences for TN (F1,4 = 0.32, P = 0.6) and P-PO4 (F1,4 = 5.26,
36 EUs subset in August 2009 and two random subsamples were P = 0.084) (Table 1). Experimentally restored marshes had
16 J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22
Table 2
Mean and standard error of surface and soil water characteristics in the experimentally restored marshes as a function of water type and water level treatments.
Parameter Irrigation water Drainage water
10 cm 20 cm 30 cm 10 cm 20 cm 30 cm
Surface water Mean 20.00 19.56 19.51 20.26 19.98 19.65
◦
temperature ( C) S.E. 0.27 0.16 0.09 0.20 0.25 0.12
Soil water temperature Mean 20.55 20.47 20.32 20.31 20.44 20.30
◦
( C) S.E. 0.05 0.07 0.17 0.23 0.20 0.15
Surface water pH Mean 7.59 7.78 7.72 7.71 7.74 7.65
S.E. 0.08 0.06 0.09 0.06 0.04 0.09
Soil water pH Mean 6.68 6.65 6.77 6.65 6.76 6.80
S.E. 0.07 0.05 0.12 0.08 0.04 0.03
Surface water DO2 Mean 5.23 5.14 5.09 5.61 4.84 4.35
−1
(mg L ) S.E. 0.59 0.35 0.43 0.54 0.26 0.77
−1
Soil water DO2 (mg L ) Mean 0.31 0.52 0.49 0.51 0.37 0.36
S.E. 0.03 0.09 0.08 0.11 0.07 0.04
Surface water Mean 1.98 1.60 1.30 1.91 1.98 1.64
−1
conductivity (mS cm ) S.E. 0.44 0.12 0.06 0.15 0.16 0.04
Soil water conductivity Mean 70.96 73.40 53.17 76.42 73.51 50.60
−1
(mS cm ) S.E. 1.39 3.49 8.20 2.54 1.54 4.26
oligohaline surface waters and hyperhaline soil waters (0.5 m negatively to higher water levels in DW treatment (Fig. 4). Plant
depth) due to saline intrusion characteristic of current conditions composition of the EUs corresponded to a oligohaline marsh veg-
within the Ebro Delta (Table 2). Experimentally restored marshes etation dominated by S. maritimus L. and S. litoralis Schrad., with
had oxygenated surface waters and sub-oxygenated soil waters high colonization by the weed P. distichum as a consequence of
(Table 2). the proximity of a rice field (Curcó, 2000). There were no signifi-
cant differences in MAB between water types (F1,26 = 1.1, P = 0.309)
3.2. Relationships between forcing and response variables
and water levels (F2,26 = 2.1, P = 0.145) nor was there a significant
block effect (F4,26 = 1.6, P = 0.192). It should be noted, however,
Principal Component Analysis results indicated a strong rela-
that the MAB data displayed an increasing trend (higher biomass)
tionship of vertical accretion with surface soil properties along
from block 1 to block 3 (area closest to an existing rice field)
component 1 (Fig. 3, top), which is explained by water type
under both water types (Fig. 4, top). This observed trend closely
variation (Fig. 3, bottom). A secondary relationship of elevation
tracked the biomass of P. distichum (Fig. 4, center). P. distichum was
change with plant biomass appears along component 2 (Fig. 3,
the most significant contributor to MAB of any other species and
top), which is explained by block variation (Fig. 3, bottom). KMO’s
was found in EUs independent of the IW or the DW treatments
measure of sampling adequacy (0.60) and Bartlett’s test of spheric-
(F1,26 = 4.1, P = 0.057) water level (F2,26 = 0.57, P = 0.571) or block
ity (P < 0.0001) indicated the appropriateness of the PCA. The first
(F4,26 = 2.1, P = 0.111). MBB was significantly different among water
two components explained a total of 43.13% of the variance, with
levels (F2,26 = 8.0, P = 0.002) and blocks (F2,26 = 3.2, P = 0.028), but not
component 1 contributing 26.89% and component 2 contributing
among water types (F1,26 = 3.5, P = 0.072). MBB only showed sig-
16.24%. An oblimin rotation was performed to aid in the inter-
nificant differences between water levels in the DW treatment for
pretation of these two components (McGarigal et al., 2000). The
pairwise comparisons (Tukey), where MBB was significantly higher
PCA rotation solution showed a number of medium (±0.40) and
in the 10 cm water level than in the 30 cm water level (P = 0.014)
high (±0.60) loadings (correlations) indicating the relationships
and higher than the 20 cm water level but not significant (P = 0.059)
of abiotic and biotic variables with vertical accretion and eleva-
(Fig. 4, bottom). A significant block effect was observed when look-
tion change in both components (Fig. 3, top). Along component 1
ing specifically at MBB in the IW treatment, where block 3 had
appears a direct relationship between vertical accretion (−0.56)
significantly higher MBB than blocks 2 and 1 (P = 0.01 and P = 0.001,
and finer grain sizes; namely clay (−0.75) and fine silt (−0.6).
respectively). In the DW treatment, block 3 had significantly higher
These variables were all opposed to soil bulk density (0.42) and
MBB than block 1 (P = 0.042) for pairwise comparisons (Tukey)
coarser grain sizes; medium silt (0.93), coarse silt (0.94) and sand
(Fig. 4, bottom).
(0.94). Component 2 shows a direct relationship between elevation
change (−0.81), MAB (−0.65) and MBB (−0.52). These variables
were all opposed to surface water pH (0.75) and DO2 (0.55), soil 3.4. Surface soil properties response among treatments
water pH (0.60) and soil bulk density (0.57). Scores of EUs explained
two main underlying factors controlling forcing and response vari- Surface soil mineral content was greater in DW treatment,
ables relationships (Fig. 3, bottom). The first factor was the water as well as bulk density, sand and silt content. Mineral con-
type variation along component 1, which explained vertical accre- tent also increased in both water type treatments with the
tion and surface soil properties relationships. The second factor was higher water levels, and decreased in blocks closer to rice field
the block variation along component 2, which explained elevation cultivation. Mineral content responded in all treatments signif-
change, plant biomass and water parameters relationships. icantly: among water types (F1,28 = 4.7, P = 0.039), water levels
(F2,28 = 4.6, P = 0.019) and blocks (F4,28 = 4.8, P = 0.004) (Fig. 5, top).
3.3. Plant biomass response among treatments Pairwise comparisons between water levels only showed sig-
nificant differences in mineral content in DW treatment: 10 cm
MAB and MBB were significantly higher in blocks closer to the with 20 cm (P = 0.04) and 30 cm (P = 0.005). Pairwise compar-
rice field due to P. distichum L colonization, and MBB also responded isons between blocks showed significant differences in mineral
J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22 17
and clay content varied inversely among water levels and blocks in
both water type treatments.
3.5. Vertical accretion and elevation change response among
treatments
Vertical accretion showed a significant increase in DW treat-
ment compared to IW treatment due to significantly higher mineral
sediment input, which promoted higher surface soil mineral con-
tent. Elevation change appeared to be affected by block effects
due to P. distichum colonization and all three parameters (ele-
vation change, MAB of P. distichum L and MBB) increased in
block 3 closest to rice cultivation. In both water type treatments,
mean values (±standard error) of vertical accretion (11.5 ± 0.8
−1
and 15.5 ± 0.6 mm yr ) were higher than those for elevation
−1
change (9.1 ± 1.4 and 8.8 ± 2.8 mm yr ). ANOVA results showed
vertical accretion was significantly higher in the DW treatment
than the IW treatment (F1,21 = 9.5, P = 0.006) (Fig. 6, top). Verti-
cal accretion did not show significant differences among water
levels (F2,21 = 0.4, P = 0.681) but showed significant differences
among blocks (F4,21 = 2.8, P = 0.05). Vertical accretion significantly
increased on blocks closer to rice field cultivation (block 3) in the
DW treatment, possibly in response to sediment capture by the
combination of higher sediment input and substantially higher
aboveground biomass of P. distichum. Block 3 displayed substan-
tially higher vertical accretion than block 1 (P = 0.075) and block
2 had significantly higher vertical accretion rates than block 1
(P = 0.05) for pairwise comparisons (Fig. 6, top). In the IW treat-
ment, vertical accretion significantly changed among blocks, where
block 3 had significantly lower accretion than block 1 (P = 0.013)
and block 2 (P = 0.034) for pairwise comparisons (Fig. 6, top).
Elevation change did not show significant differences among
water types (F1,16 = 0.1, P = 0.797) and water levels (F2,16 = 0.1,
P = 0.868) but it showed significant differences among blocks
(F4,16 = 4.2, P = 0.016) (Fig. 6, bottom). Particularly, block 3 in both
water type treatments had higher elevation change (11.3 ± 2.3
−1
and 17.8 ± 2.9 mm yr ) than vertical accretion (8.3 ± 1.3 and
−1
15.1 ± 1.3 mm yr ). This positive difference when subtracting ver-
tical accretion rates from elevation change rates points out that
significantly higher belowground biomass in block 3 also con-
tributed to elevation change by root growth due to high weed
colonization by P. distichum from rice field edge. Block 3 of the DW
treatment had significantly higher rates of elevation change than
either block 2 or 1 (P = 0.043 and P = 0.042, respectively) for pair-
wise comparisons (Fig. 6, bottom). In the IW treatment, elevation
change did not show any significant differences between blocks
Fig. 3. Principal Component Analysis of the forcing and response variables. Factor although it displayed an increasing trend from the block 1 to the
loadings of the variables (top) and scores of experimental units classified by water block 3 (Fig. 6, bottom).
type treatments and block effects (bottom).
4. Discussion
content in both water type treatments. Block 3 had significantly
lower mineral content than block 1 (P = 0.02) in the IW treat- Marsh development and stability are dependent on allogenic
ment. Block 2 had significantly lower mineral content than block (e.g. flooding, sediment inputs) and autogenic factors (e.g. plant
1 (P = 0.04). There were significant differences in bulk density growth) (Singer et al., 1996; Waller et al., 1999). Initial stages of
between water types (F1,28 = 12.9, P = 0.001) but not between marsh succession are usually controlled by mineral contributions
water levels (F2,28 = 1.1, P = 0.365) and blocks (F4,28 = 0.1, P = 0.979) that control the optimal elevation to favor vegetation coloniza-
(Fig. 5, center). There were no significant differences for any par- tion and development (Morris et al., 2002). Mature marshes may
ticle size content between water types, water levels and blocks have greater organic contribution (e.g. leaf litter deposition and
(Fig. 5, bottom): sand (F1,28 = 1.7, P = 0.205; F2,28 = 1.5, P = 0.249; and root growth) because a more extensive plant community cover is
F4,28 = 2.4, P = 0.071), silt (F1,28 = 2.4, P = 0.129; F2,28 = 1.1, P = 0.338; developed and marsh elevation gain causes higher isolation from
and F4,28 = 2.9, P = 0.061) and clay (F1,28 = 3.8, P = 0.062; F2,28 = 0.8, marine and riverine sediment sources (Brinson et al., 1995; Mitsch
P = 0.462; and F4,28 = 2.5, P = 0.082). Two general trends of particle and Gosselink, 2007). Under a sediment-deficit scenario, autogenic
size content appeared among treatments. First, both sand and silt organic contributions may be critical to marsh stability and survival
increased in DW treatment inversely to clay content. Secondly, silt to support the balance between elevation gain and RSLR (DeLaune
18 J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22
Fig. 4. Partly nested ANOVA results of mean (±SE) plant biomass response among water types, water levels and blocks. Where there were significant main effects (˛ = 0.05)
on ANOVA results among water levels and block effects, Tukey pairwise comparisons were tested within each water type treatment and different letters denotes significant
differences.
and Pezeshki, 2003; Blum and Christian, 2004; Nyman et al., 2006; gain, especially when the weed P. distichum colonized rapidly and
Langley et al., 2009; Kirwan and Guntenspergen, 2012). In our densely the experimentally restored marshes. The observed overall
study, mineral contributions controlled vertical accretion and ele- mean rates of vertical accretion and elevation change also support
vation change in the establishment of oligohaline restored marshes the hypothesis that oligohaline restored marshes often have eleva-
even under sediment-deficit conditions. Higher mean vertical tion gains higher than RSLR in the Ebro Delta, at least during the
−1
accretion rates (11.5 ± 0.8 and 15.5 ± 0.6 mm yr ) than elevation initial phase of marsh establishment.
−1
change (9.1 ± 1.4 and 8.8 ± 2.8 mm yr ) in both water type treat- Vertical accretion responded positively to higher mineral input
ments suggests that the surface accretion processes via mineral from the rice field drainage water but vertical accretion was not
sedimentation overall controlled marsh elevation. However, sub- affected by plant colonization among blocks. Our results show a
soil expansion via root growth also caused a positive elevation significant higher surface soil mineral content in DW treatment due
J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22 19
Fig. 5. Partly nested ANOVA results of mean (±SE) surface soil properties response among water types, water levels and blocks. An asterisk indicates significant increase
˛
( = 0.05) between water type treatments. Where there were significant main effects (˛ = 0.05) on ANOVA results among water levels and block effects, Tukey pairwise
comparisons were tested within each water type treatment and different letters denotes significant differences.
to significant higher mineral input that contributes significantly to organic contribution to marsh elevation. An alternative explana-
vertical accretion. The multivariate analysis results also pointed out tion is that agricultural run-off may also contain herbicides, which
the strong relationship between vertical accretion and surface soil may reduce plant germination (Reynoldson and Zarull, 1993; Jurik
mineral properties along the component 1, which was explained et al., 1994). The use of herbicides in rice fields of the Ebro Delta such
by primary source of variation due to water type treatments. Sim- as molinate, propanil and 2–4 MCP is the most common way to con-
ilar plant growth in both water type treatments and lower surface trol weeds (Echinochloa spp., Cyperus spp. and Scirpus spp.; Manosa˜
soil organic content in the DW treatment may indicate that higher et al., 2001), so herbicide content in DW treatment could also affect
nutrient levels from drainage waters did not enhance accretion via plant communities of the experimentally restored marshes.
organic contribution as several studies have already pointed out We also hypothesize that P. Distichum enhanced positive eleva-
(Craft and Richardson, 1993; Rybczyk et al., 2002; Brantley et al., tion change rates via fast root growth in the initial stages of the
2008). A possible explanation is that small differences in nutrient experimentally restored marsh development (i.e. within the first
content between water type inflows may require a longer time of three years) (Anderson and Ehringer, 2000; Wanyama et al., 2012).
fertilization to cause differences in plant growth and subsequent Both elevation change and MBB increased significantly in blocks
20 J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22
Fig. 6. ANOVA results of mean (±SE) vertical accretion and elevation change response among water types, water levels and blocks. An asterisk indicates significant increase
(˛ = 0.05) between water type treatments. Where there were significant main effects (˛ = 0.05) on ANOVA results among water levels and block effects, Tukey pairwise
−1
comparisons were tested within each water type treatment and different letters denotes significant differences. The dashed line represents global (3 mm yr ) and regional
−1
projections (5 mm yr ) of ESLR means (IPCC, 2007; Marcos and Tsimplis, 2008). The shaded area represents predicted RSLR for the Ebro Delta (Ibánez˜ et al., 2010).
closest to rice cultivation (block 3), where P. distichum colonization Europe, Asia and the Pacific (Curcó, 2000; CABI, 2012). Though
appears to originate from the earth berm edge that divided the a vigorous invader of newly reclaimed marshland, this species is
adjacent rice field and the experimental study. The multivariate documented to be a minor contributor in natural and restored
analysis results also pointed out this strong relationship between oligohaline marshes in mature succession stages (Comín et al.,
elevation change and both MAB and MBB along the component 2, 2001; Curcó, 2001). These findings suggest that initial invasions
which was explained by a secondary source of the variation due to by this plant in the restored marshes (at least in the Ebro Delta)
block effects. On close examination, our results also point out that should not be of great concern and perhaps even encouraged when
water levels may indirectly control elevation change influencing the overarching goal of the marsh restoration is RSLR abatement
root growth in DW treatment. Prolonged higher water levels dur- and passive water treatment.
ing the experiment may have caused a physiological stress reducing Previous works have highlighted marsh ecosystems services
root productivity in higher water levels (Mendelssohn and Morris, providing coastal protection to human populations against storm
2000). Both elevation change and MBB increased significantly with surges and RSLR (Gedan et al., 2011; Shepard et al., 2011). Our
lower water levels in the DW treatment. Oppositely, there was a study strongly supports the use of restored marshes as natural
30% decrease of soil water DO2 from 10 cm to 30 cm water level buffers against RSLR. Experimentally restored marshes receiving
treatment that may reduce root growth. Finally, root growth could rice field drainage water balanced RSLR rates due to a combination
not affect vertical accretion rates because most of root growth may of a significant mineral contribution (sediment input) to verti-
have occurred below the placed marker horizons and may only cal accretion and high organic contribution (root production) to
affect elevation change (Cahoon et al., 1999, 2006). elevation change. To note, the experimentally restored marshes
Our results support the idea that wetland restoration initiatives had higher overall mean values in both water type treatments of
−1
with the primary goal of maximize marsh elevation gain should vertical accretion (11.5 ± 0.8 and 15.5 ± 0.6 mm yr ) and eleva-
−1
consider the inclusion of vegetated buffers to mitigate or pro- tion change (9.1 ± 1.4 and 8.8 ± 2.8 mm yr ) than brackish natural
mote the edge effects of plant colonization (Murcia, 1995; Wu and marshes in the Ebro Delta. For example, in riverine sites, the aver-
Mitsch, 1998; Feagin and Wu, 2006). Interestingly, P. distichum is age rate of vertical accretion and elevation change were 5.03 ± 0.33
−1
considered a major weed of rice fields and restored marshes in and 6.61 ± 2.36 mm yr , respectively (Ibánez˜ et al., 2010).
J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22 21
Vertical accretion and elevation change rates in the experimentally Chen, C.C., McCarl, B., Chang, C.C., 2012. Climate change, sea level rise and rice: global
market implications. Clim. Change 110, 543–560.
restored marshes were also overall higher than in other brackish
Comín, F.A., Romero, J.A., Hernandez, O., Menendez, M., 2001. Restoration of
natural marshes located in Northwestern Mediterranean Deltas
wetlands from abandoned rice fields for nutrient removal, and biological com-
−1
± ±
such as the Po Delta (10.7 4.2 and 7.3 2.1 mm yr , respec- munity and landscape diversity. Restor. Ecol. 9, 201–208.
−
1 Craft, C., 2007. Freshwater input structures soil properties, vertical accretion, and
tively) and the Rhône Delta (12.5 ± 3.2 and 11.4 ± 3.2 mm yr ,
nutrient accumulation of Georgia and U.S. tidal marshes. Limnol. Oceanogr. 52,
respectively) (Day et al., 2011). These findings suggest that exper- 1220–1230.
imentally restored marshes result on higher vertical accretion and Craft, C.B., Richardson, C.J., 1993. Peat accretion and N, P, and organic C accumu-
lation in nutrient-enriched and unenriched Everglades Peatlands. Ecol. Appl. 3,
elevation change rates than natural marshes because of water
446–458.
input and turnover was large enough to favor sedimentation even
Cronk, J.K., Siobhan Fennessy, M., 2001. Wetland Plants. CRC Press, Boca Raton, FL.
under low suspended sediment availability. Using freshwater in Curcó, A., 2000. La vegetació del delta de l’Ebre (IV): Les comunitats nitrófies. Acta
marsh restoration projects located in sediment-deficient deltas Bot. Barc. 46, 143–178.
Curcó, A., 2001. The vegetation of the Ebro Delta (V): helophytic and hygrophilous
and estuaries has the potential to be a positive option for the
communities. Lazaroa 22, 67–81.
main restoration goals seeking to mitigate RSLR, since freshwater
Curcó, A., Canicio, A., Ibánez,˜ C., 1995. Mapa d’habitats potencials del delta de l’Ebre.
may enhance vertical accretion and elevation change via auto- Butlletí del Parc Nat. Delta Ebre 9, 4–12.
Curcó, A., Ibánez,˜ C., Day, J.W., Prat, N., 2002. Net primary production and decompo-
genic organic matter production (Nyman et al., 2006; Craft, 2007;
sition of salt marshes of the Ebre delta (Catalonia, Spain). Estuaries 25, 309–324.
Neubauer, 2008).
Day, J., Ibánez,˜ C., Scarton, F., Pont, D., Hensel, P., Day, J., Lane, R., 2011. Sustaina-
bility of Mediterranean Deltaic and Lagoon Wetlands with sea-level rise: the
importance of river input. Est. Coasts 34, 483–493.
Acknowledgements
Day, J.W., Christian, R.R., Boesch, D.M., Yanez-Arancibia, A., Morris, J., Twilley, R.R.,
Naylor, L., Schaffner, L., Stevenson, C., 2008. Consequences of climate change on
the ecogeomorphology of coastal wetlands. Est. Coasts 31, 477–491.
This study has been funded by the Government of Spain
Day Jr., J.W., Boesch, D.F., Clairain, E.J., Kemp, G.P., Laska, S.B., Mitsch, W.J., Orth,
(Ministerio de Medio Ambiente, Research Project 056/RN08/04.3,
K., Mashriqui, H., Reed, D.J., Shabman, L., Simenstad, C.A., Streever, B.J., Twilley,
development of techniques to compensate subsidence and sea- R.R., Watson, C.C., Wells, J.T., Whigham, D.F., 2007. Restoration of the Mississippi
Delta: lessons from Hurricanes Katrina and Rita. Science 315, 1679–1684.
level rise in coasts and wetlands of the Ebro Delta, 2009–2011). We
DeLaune, R.D., Jugsujinda, A., Peterson, G.W., Patrick, W.H., 2003. Impact
would like to thank Lluis Jornet, David Mateu, Rosa Valmana˜ and
of Mississippi River freshwater reintroduction on enhancing marsh
Dr. Walter Tzilkowski for technical support and assistance in field- accretionary processes in a Louisiana estuary. Est. Coast. Shelf Sci. 58,
653–662.
work and lab analysis. We also thank three anonymous reviewers
DeLaune, R.D., Pezeshki, S.R., 2003. The role of soil organic carbon in maintaining
for constructive comments helped us to improve this manuscript.
surface elevation in rapidly subsiding U.S. Gulf of Mexico coastal marshes. Water
Air Soil Pollut.: Focus 3, 167–179.
DMAiH, 2008. Framework Study N1: Ebro Delta. Framework Studies for Later Use in
Appendix A. Supplementary data
Defining a Strategy for Preventing and Adapting to Climate Change in Catalonia.
Departament de Medi Ambient i Habitatge, Barcelona, Spain.
Supplementary data associated with this article can be Fagherazzi, S., Kirwan, M.L., Mudd, S.M., Guntenspergen, G.R., Temmerman, S.,
D’Alpaos, A., van de Koppel, J., Rybczyk, J.M., Reyes, E., Craft, C., Clough, J., 2012.
found, in the online version, at http://dx.doi.org/10.1016/j.ecoleng.
Numerical models of salt marsh evolution: ecological, geomorphic, and climatic
2013.09.047.
factors. Rev. Geophys., 50.
Feagin, R.A., Wu, X.B., 2006. Spatial pattern and edge characteristics in restored ter-
race versus reference salt marshes in Galveston Bay. Wetlands 26, 1004–1011.
References
FitzGerald, D.M., Fenster, M.S., Argow, B.A., Buynevich, I.V., 2008. Coastal impacts
due to sea-level rise. Annu. Rev. Earth Planet Sci. 36, 601–647.
AENOR, 1996. Norma UNE-EN 872. Water Quality. Determination of Total Suspended Gedan, K.B., Kirwan, M.L., Wolanski, E., Barbier, E.B., Silliman, B.R., 2011. The present
Solids. AENOR, Madrid. and future role of coastal wetland vegetation in protecting shorelines: answer-
Alvarado-Aguilar, D., Jimenez, J.A., Nicholls, R.J., 2012. Flood hazard and damage ing recent challenges to the paradigm. Clim. Change 106, 7–29.
assessment in the Ebro Delta (NW Mediterranean) to relative sea level rise. Nat. Grasshoff, K., Ehrhardt, M., Kremling, K., 1999. Methods of Seawater Analysis. Verlag
Hazards 62, 1301–1321. Chemie, Weinheim.
Anderson, J., Ehringer, J.N., 2000. Ecological uses for Paspalum vaginatum (Swartz) Ibánez,˜ C., Bertolero, A., 2009. Delta Lagoon. Technical Application Form. LIFE+
seashore paspalum. In: Cannizzaro, P.J. (Ed.), Twenty Seventh Annual Confer- Nature & Biodiversity, European Union.
ence on Ecosystem Restoration and Creation. Ibánez,˜ C., Canicio, A., Day, J., Curcó, A., 1997. Morphologic development, relative
Blum, L.K., Christian, R.R., 2004. Belowground production and decomposition along sea level rise and sustainable management of water and sediment in the Ebre
a tidal gradient in a Virginia salt marsh. In: Fagherazzi, S., Marani, M., Blum, L.K. Delta, Spain. J. Coastal Conserv. 3, 191–202.
(Eds.), The Ecogeomorphology of Tidal Marshes, vol. 59. AGU, Washington, DC, Ibánez,˜ C., Prat, N., 2003. The environmental impact of the Spanish National Hydro-
p. 268. logical Plan on the lower Ebro River and delta. Int. J. Water Resources Dev. 19,
Brantley, C.G., Day, J.W., Lane Jr., R.R., Hyfield, E., Day, J.N., Ko, J.-Y., 2008. Primary 485–500.
production, nutrient dynamics, and accretion of a coastal freshwater forested Ibánez,˜ C., Prat, N., Canicio, A., 1996. Changes in the hydrology and sediment trans-
wetland assimilation system in Louisiana. Ecol. Eng. 34, 7–22. port produced by large dams on the lower Ebro river and its estuary. Regul.
Brinson, M.M., Christian, R.R., Blum, L.K., 1995. Multiple states in the sea-level Rivers-Res. Manag. 12, 51–62.
induced transition from terrestrial forest to estuary. Estuaries 18, 648–659. Ibánez,˜ C., Sharpe, P.J., Day, J.W., Day, J.N., Prat, N., 2010. Vertical accretion and rel-
CABI, 2012. Paspalum ditichum. In: Invasive Species Compendium. CAB International, ative sea level rise in the Ebro Delta Wetlands (Catalonia, Spain). Wetlands 30,
Wallingford, UK. 979–988.
Cahoon, D.R., Turner, R.E., 1989. Accretion and canla impacts in rapidly subsiding IBM, 2010. IBM SPSS Advanced Statistics 19. IBM.
wetal. 2. Feldspar marker horizon technique. Estuaries 12, 260–268. IPCC, 2007. In: Pachauri, R.K., Reisinger, A. (Eds.), Climate Change 2007. Synthesis
Cahoon, D., Day, J., Reed, D.J., 1999. The influence of surface and shallow sub- Report: Contribution of Working Groups I, II and III to the Fourth Assess-
surface soil processes on wetland elevation: a synthesis. Curr. Top. Wetland ment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva,
Biogeochem. 3, 72–88. Switzerland.
Cahoon, D., Hensel, Spencer, T., Reed, D.J., McKee, K.L., Saintilan, N., 2006. Coastal ISO11277, 2002. Soil Quality – Determination of Particle Size Distribution in Mineral
wetland vulnerability to relative sea level rise: wetland elevation trends and Soil Material – Method by Sieving and Sedimentation. Beuth-Verlag, Berlin.
process controls. In: Verhoeven, J.T.A., Beltman, B., Bobbink, R., Whigham, D. Jurik, T.W., Wang, S.C., Vandervalk, A.G., 1994. Effects of sediment load on seedling
(Eds.), Wetlands and Natural Resource Management, vol. 190. Springer, Berlin emergence from Wetland Seed Banks. Wetlands 14, 159–165.
and New York, pp. 271–292. Kirwan, M.L., Guntenspergen, G.R., 2012. Feedbacks between inundation, root pro-
Cahoon, D.R., Lynch, J.C., Perez, B.C., Segura, B., Holland, R.D., Stelly, C., Stephenson, G., duction, and shoot growth in a rapidly submerging brackish marsh. J. Ecol. 100,
Hensel, P., 2002. High-precision measurements of wetland sediment elevation: 764–770.
II. The rod surface elevation table. J. Sediment. Res. 72, 734–739. Langley, J.A., McKee, K.L., Cahoon, D.R., Cherry, J.A., Megonigal, J.P., 2009. Elevated
Cardoch, L., Day, J.W., Ibánez,˜ C., 2002. Net primary productivity as an indicator of CO2 stimulates marsh elevation gain, counterbalancing sea-level rise. Proc. Natl.
sustainability in the Ebro and Mississippi deltas. Ecol. Appl. 12, 1044–1055. Acad. Sci. U.S.A. 106, 6182–6186.
Carr, C., 2010. Plant Fact Sheet for Knotgrass (Paspalum distichum). USDA-Natural Manosa,˜ S., Mateo, R., Guitart, R., 2001. A review of the effects of agricultural and
Resources Conservation Service, James E. “Bud” Smith Plant Materials Center, industrial contamination on the Ebro delta biota and wildlife. Environ. Monit.
Knox City, TX, pp. 79529. Assess. 71, 187–205.
22 J. Calvo-Cubero et al. / Ecological Engineering 61 (2013) 12–22
Marcos, M., Tsimplis, M.N., 2008. Comparison of results of AOGCMs in the Mediter- Reynoldson, T.B., Zarull, M.A., 1993. An approach to the development of biologi-
ranean Sea during the 21st century. J. Geophys. Res.-Oceans, 113. cal sediment guidelines. In: Woodley, S., Kay, J., Francis, G. (Eds.), Ecological
MARM, 2006. Plan Integral de Protección del Delta del Ebro. Documento Base. Mini- Integrity and the Management of Ecosystems. St. Lucie Press, Delray Beach, FL,
sterio de Medio Ambiente, Madrid. pp. 177–200.
Martinez-Vilalta, A., 1995. The rice fields of the Ebro Delta. In: Morillo, C., González, Rybczyk, J.M., Day, J.W., Conner, W.H., 2002. The impact of wastewater effluent
J.L. (Eds.), Management of Mediterranean Wetlands. Ministerio de Medio Ambi- on accretion and decomposition in a subsiding forested wetland. Wetlands 22,
ente, Madrid. 18–32.
McGarigal, K., Cushman, S., Stafford, S., 2000. Multivariate Statistics for Wildlife and Schubauer, J.P., Hopkinson, C.S., 1984. Above-ground and belowground emergent
Ecological Research. Springer-Verlag, New York. macrophyte production and turnover in a coastal marsh ecosystem, Georgia.
McKee, K.L., Mendelssohn, I.A., 1989. Response of a fresh-water marsh plant com- Limnol. Oceanogr. 29, 1052–1065.
munity to increased salinity and increased water level. Aquat. Bot. 34, 301–316. Schurman, J.J., Goedewaagen, M.A.L., 1971. Methods for Experiment Root Systems
Mendelssohn, I.A., Morris, J.T., 2000. Eco-physiological control on the productivity and Roots. Wageningen Pudoc, Netherlands.
of Spartina alterniflora loisel. In: Kreeger, M.P.W.a.D.A. (Ed.), Concepts and Con- Seo/BirdLife, 1997. Pla Delta. XXI. Directrices para la conservación y desarrollo
troversies in Tidal Marsh Ecology. Kuwer Academic Publishers, Dortrecht, The sostenible en el Delta del Ebro. Seo/BirdLife, Madrid.
Netherlands. Shepard, C.C., Crain, C.M., Beck, M.W., 2011. The protective role of coastal marshes:
Mitsch, W.J., Gosselink, J.G., 2007. Wetlands. John Wiley and Sons Ltd., New York. a systematic review and meta-analysis. PLoS ONE 6, 11.
Morris, J.T., Sundareshwar, P.V., Nietch, C.T., Kjerfve, B., Cahoon, D.R., 2002. Singer, D.K., Jackson, S.T., Madsen, B.J., Wilcox, D.A., 1996. Differentiating climatic
Responses of coastal wetlands to rising sea level. Ecology 83, 2869–2877. and successional influences on long-term development of a marsh. Ecology 77,
Murcia, C., 1995. Edge effects in fragmented forests – implications for conservation. 1765–1778.
Trends Ecol. Evol. 10, 58–62. Syvitski, J.P.M., Kettner, A.J., Overeem, I., Hutton, E.W.H., Hannon, M.T., Brakenridge,
Neubauer, S.C., 2008. Contributions of mineral and organic components to tidal G.R., Day, J., Vorosmarty, C., Saito, Y., Giosan, L., Nicholls, R.J., 2009. Sinking deltas
freshwater marsh accretion. Est. Coast. Shelf Sci. 78, 78–88. due to human activities. Nat. Geosci. 2, 681–686.
Nyman, J.A., Walters, R.J., Delaune, R.D., Patrick Jr., W.H., 2006. Marsh vertical accre- Waller, M.P., Long, A.J., Long, D., Innes, J.B., 1999. Patterns and processes in the
tion via vegetative growth. Est. Coast. Shelf Sci. 69, 370–380. development of coastal mire vegetation: multi-site investigations from Walland
Page, A.L., Miller, R.H., Keeny, D.R., 1982. Methods of Soil Analysis. American Society Marsh, Southeast England. Quater. Sci. Rev. 18, 1419–1444.
of Agronomy, Madison, WI. Wanyama, J., Herremans, K., Maetens, W., Isabirye, M., Kahimba, F., Kimaro, D., Poe-
Pont, D., Day, J.W., Hensel, P., Franquet, E., Torre, F., Rioual, P., Ibánez,˜ C., Coulet, sen, J., Deckers, J., 2012. Effectiveness of tropical grass species as sediment filters
E., 2002. Response scenarios for the deltaic plain of the Rhone in the face of an in the riparian zone of Lake Victoria. Soil Use Manag. 28, 409–418.
acceleration in the rate of sea-level rise with special attention to Salicornia-type Wu, X.Y., Mitsch, W.J., 1998. Spatial and temporal patterns of algae in newly con-
environments. Estuaries 25, 337–358. structed freshwater wetlands. Wetlands 18, 9–20.
Quinn, G.P., Keough, M.J., 2002. Experimental Design and Data Analysis for Biologists.
Cambridge University Press, New York.