Restored intertidal eelgrass (Z. marina) supports benthic communities taxonomically and functionally similar to natural seagrasses in the Wadden Sea

Abstract

Ecological restoration has become an important management-tool to counteract the widespread losses of seagrass meadows and their associated biodiversity. In the Dutch Wadden Sea, long-term restoration efforts have recently led to the successful restoration of annual eelgrass (Zostera marina) at high densities on a local scale. However, it is yet unknown if restored seagrass plants also lead to improved local biodiversity and ecosystem functioning in the intertidal zone. We therefore compared the macrozoobenthos communities of a small-scale restored meadow to 22 naturally occurring intertidal seagrass meadows. Using a taxonomic and trait-based approach we aimed to study 1) how intertidal seagrasses (Zostera marina and Zostera noltii) affect benthic communities and their functional trait distribution and 2) if a restored meadow facilitates benthic communities similar to natural meadows. We found that both natural and restored seagrasses increased abundances of benthic animals and the richness (both taxonomic and functional) of associated benthic communities compared to nearby unvegetated areas. Additionally, the presence of intertidal seagrass shifted benthic community composition both taxonomically and functionally, thus broadening the niche space for species inhabiting tidal flats. Seagrasses especially facilitated epifaunal species and traits associated with these animals. Surprisingly, our results indicate that the mere presence of seagrass aboveground structure is enough to facilitate benthic communities, as neither higher seagrass cover nor biomass increased benthic biodiversity in the intertidal zone. By studying the effect of seagrass restoration on benthic diversity, we found that the restored meadow functioned similarly to the natural meadows after only two years and that the success of our restoration efforts indeed led to local biodiversity enhancements. Our findings contribute to the understanding of the ecological functioning of intertidal seagrasses and can be used to define/refine conservation and restoration goals of these valuable ecosystems.

Full text

Restored intertidal eelgrass
(Z. marina) supports benthic
communities taxonomically and
functionally similar to natural
seagrasses in the Wadden Sea
Max L. E. Gräfnings
1,2
*, Ise Grimm
1
, Stephanie R. Valdez
3
,
India Findji
1
, Tjisse van der Heide
1,2,4
, Jannes H. T. Heusinkveld
5
,
Kasper J. Meijer
1
, Britas Klemens Eriksson
1
, Quirin Smeele
6
and Laura L. Govers
1,2,4
1
Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences (GELIFES), University
of Groningen, Groningen, Netherlands,
2
Department of Aquatic Ecology and Environmental Biology,
Institute for Water and Wetland Research (IWWR), Radboud University, Nijmegen, Netherlands,
3
Division of Marine Science, Nicholas School of the Environment, Duke University, Beaufort,
NC, United States,
4
Department of Coastal Systems, Royal Netherlands Institute for Sea Research
(NIOZ), Den Burg, Netherlands,
5
The Fieldwork Company, Groningen, Netherlands,
6
Natuurmonumenten, Paterswolde, Netherlands
Ecological restoration has become an important management-tool to counteract
the widespread losses of seagrass meadows and their associated biodiversity. In the
Dutch Wadden Sea, long-term restoration efforts have recently led to the successful
restoration of annual eelgrass (Zostera marina) at high densities on a local scale.
However, it is yet unknown if restored seagrassplantsalsoleadtoimprovedlocal
biodiversity and ecosystem functioning in the intertidal zone. We therefore
compared the macrozoobenthos communities of a small-scale restored meadow
to 22 naturally occurring intertidal seagrass meadows. Using a taxonomic and trait-
based approach we aimed to study 1) how intertidal seagrasses (Zostera marina and
Zostera noltii) affect benthic communities and their functional trait distribution and 2)
if a restored meadow facilitates benthic communities similar to natural meadows. We
found that both natural and restored seagrasses increased abundances of benthic
animals and the richness (both taxonomic and functional) of associated benthic
communities compared to nearby unvegetated areas. Additionally, the presence of
intertidal seagrass shifted benthic community composition both taxonomically and
functionally, thus broadening the niche space for species inhabiting tidal flats.
Seagrasses especially facilitated epifaunal species and traits associated with these
animals. Surprisingly, our results indicate that the mere presence of seagrass
aboveground structure is enough to facilitate benthic communities, as neither
higher seagrass cover nor biomass increased benthic biodiversity in the intertidal
zone. By studying the effect of seagrass restoration on benthic diversity, we found
that the restored meadow functioned similarly to the natural meadows after only two
years and that the success of our restoration efforts indeed led to local biodiversity
enhancements. Our findings contribute to the understanding of the ecological
functioning of intertidal seagrasses and can be used to define/refine conservation
and restoration goals of these valuable ecosystems.
KEYWORDS
seagrass, ecological restoration, biodiversity, Wadden Sea, functional diversity, macrozoobenthos
Frontiers in Marine Science frontiersin.org01
OPEN ACCESS
EDITED BY
Shaochun Xu,
Chinese Academy of Sciences (CAS), China
REVIEWED BY
Arnaldo Marı
´n,
University of Murcia, Spain
Jennifer Li Ruesink,
University of Washington, United States
*CORRESPONDENCE
Max L. E. Gräfnings
maxgrafnings@gmail.com
RECEIVED 15 September 2023
ACCEPTED 31 December 2023
PUBLISHED 18 January 2024
CITATION
Gräfnings MLE, Grimm I, Valdez SR, Findji I,
van der Heide T, Heusinkveld JHT, Meijer KJ,
Eriksson BK, Smeele Q and Govers LL (2024)
Restored intertidal eelgrass (Z. marina)
supports benthic communities taxonomically
and functionally similar to natural
seagrasses in the Wadden Sea.
Front. Mar. Sci. 10:1294845.
doi: 10.3389/fmars.2023.1294845
COPYRIGHT
© 2024 Gräfnings, Grimm, Valdez, Findji,
van der Heide, Heusinkveld, Meijer, Eriksson,
SmeeleandGovers.Thisisanopen-access
article distributed under the terms of the
Creative Commons Attribution License (CC BY).
The use, distribution or reproduction in other
forums is permitted, provided the original
author(s) and the copyright owner(s) are
credited and that the original publication in
this journal is cited, in accordance with
accepted academic practice. No use,
distribution or reproduction is permitted
which does not comply with these terms.
TYPE Original Research
PUBLISHED 18 January 2024
DOI 10.3389/fmars.2023.1294845

1 Introduction
Seagrasses are marine flowering plants that form vast
underwater meadows in coastal waters worldwide. In addition to
being some of the most productive ecosystems in the world (Duarte
and Chiscano, 1999), these meadows provide essential ecosystem
services and contribute to climate change mitigation. For instance,
seagrass meadows provide vital nursery habitats for commercially
important species, offer coastal protection, and sequester large
amounts of carbon (Nordlund et al., 2016). Additionally, seagrass
meadows are generally regarded as diversity hotspots, serving as
crucial habitats to a wide array of animals, from charismatic mega
herbivores to microscopic critters. However, seagrasses are seriously
threatened and during the last century an estimated ~29% of the
global seagrass area was lost (Orth et al., 2006;Waycott et al., 2009).
Ecological restoration has become an important management-
tool, supplementing traditional passive conservation efforts, to
counteract declines of seagrasses and other coastal ecosystems.
However, coastal ecosystem restoration is still in its infancy and
often challenging in practice (Bayraktarov et al., 2016). The reasons
hindering successful coastal restoration are many, ranging from
practical methodological problems to how the public perceives
marine ecosystem restoration (Suding, 2011;Bayraktarov et al.,
2016;Abelson et al., 2020). One specific aspect that is often lacking
is how restoration success is defined and measured (Abelson et al.,
2020). Success is often defined solely based on how the restoration
effort affects the target species (Suding, 2011). Although useful as a
short-term indicator of success, this is generally an insufficient
approach since ecological restoration is about restoring ecosystem
integrity and associated ecosystem functions (Suding et al., 2015).
Hence, there is a need for monitoring programs to also measure
restoration success beyond the target species. To evaluate the
success of a restoration project, The Society of Ecological
Restoration (SER, 2004;Gann et al., 2019) recommends assessing
nine ecosystem attributes including biodiversity, resilience and self-
sustainability. Ideally, restoration projects would follow these
guidelines, but in reality, monitoring all the proposed ecosystem
attributes requires more funds and long-term commitment than
restoration projects usually have available. Thus, measurements
that combine feasibility with information about the overall
performance of the restored ecosystems are urgently needed.
In the Wadden Sea, seagrasses experienced large declines during
the 20th century. Vast subtidal eelgrass (Zostera marina) meadows
vanished completely in the 1930s, due to the seagrass wasting
disease and coastal development (den Hartog and Polderman,
1975;Giesen et al., 1990). Intertidal seagrass populations
persisted, but were heavily diminished by increased
eutrophication in the 1970s and 80s (van Katwijk et al., 2010).
During the last decades, intertidal meadows have recovered in the
northern Wadden Sea (Dolch et al., 2013), but in the south
(Netherlands and Lower Saxony) recovery has remained almost
entirely absent (Dolch et al., 2017). Today, only intertidal
seagrasses, perennial dwarf eelgrass (Zostera noltii) and annual
common eelgrass (Z. marina), persist in the Wadden Sea. The
loss of seagrass meadows has affected the ecosystem functioning
and biodiversity of the sea. For instance, seagrass declines have
altered sediment dynamics, increased water turbidity, led to the loss
of commercially important nursery habitats and reduced food
availability for herbivorous birds (Wolff, 1979;Ganter, 2000;Polte
et al., 2005;van der Heide et al., 2007;Eriksson et al., 2010).
During the last decades, seagrass restoration efforts have been
performed in the Dutch Wadden Sea (e.g., van Katwijk et al., 2009;
van Duren and Van Katwijk, 2015;Govers et al., 2022), with the
goal to counteract the widespread seagrass losses and to recover lost
ecosystem functions. Recently, the persistent restoration efforts
have started to pay off, as we have been able to restore high
densities of Z. marina on relatively large areas (2664 m² in 2020
and 1 ha in 2021, Gräfnings et al., 2023 & unpublished results) using
a newly developed seeding method (DIS-method; Govers et al.,
2022;Gräfnings et al., 2022). However, to properly evaluate if the
restoration has been successful, further monitoring is needed to
confirm that the efforts have also enhanced ecosystem integrity
beyond the target species.
In this paper we investigate how seagrass restoration affects
benthic communities as an indicator of the degree of restoration
success (Dolbeth et al., 2013;Lefcheck et al., 2017).
Macrozoobenthic communities are the foundation of many
ecosystem services in benthic systems (Snelgrove, 1999).
Macrozoobenthic animals can affect their surroundings in
multiple ways, from nutrient recycling and oxygenation of
sediments to grazing and stabilization of sediments (see review by
Levin et al., 2001). Furthermore, many benthic animals function as
crucial food resources for higher trophic levels and can thus offer
information about cross-ecosystem dynamics. Hence, studying
benthic communities can offer valuable information about how
restoration efforts affect local biodiversity and ecosystem
functioning, especially if complementary taxonomic and
functional diversity approaches are used in parallel (Henseler
et al., 2019). Traditional taxonomic diversity approaches base
their results on species identities, while functional diversity is
usually measured through species traits (Violle et al., 2007) and is
considered a good predictor of ecosystem function (Cadotte et al.,
2011). However, before the effect of the restored seagrass on benthic
communities can be properly evaluated in the Wadden Sea,
accurate information is needed about how natural seagrass
meadows affect benthic communities in the area. Although the
effect of seagrasses on benthic diversity (both taxonomic and
functional) is well studied (e.g., Orth et al., 1984;Boström and
Bonsdorff, 1997;Lefcheck et al., 2017;Boyeet al., 2019), little is
known about how intertidal seagrasses affect benthic diversity
(especially functional diversity) in the Wadden Sea or in restored
seagrass beds.
In this study, we assess 1) how intertidal seagrass (annual Z.
marina and/or perennial Z. noltii) presence affect taxonomic and
functional diversity (richness, evenness) and community structure
(composition) of macrozoobenthos and 2) whether a recently
restored Z. marina meadow affects the associated benthic
community similar to natural meadows in the intertidal Wadden
Sea. We expect intertidal seagrasses to generally facilitate
biodiversity, but that the two seagrass species might affect benthic
communities differently due to differences in structural attributes
and life cycle. For instance, the yearly turnover of annual Z. marina
Gräfnings et al. 10.3389/fmars.2023.1294845
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is expected to affect benthic community composition differently
than more stable perennial seagrasses like Z. noltii. We hypothesize
that mobile benthic species will benefit the most from the short life
cycle of annual Z. marina. Additionally, only Z. noltii forms
traditional seagrass ‘meadows’in the Wadden Sea, while
monospecificannualZ. marina populations spread out very
sparsely (<1 plant/m²) over large areas (personal observation;
Figure 1D). The ability of seagrass meadows to shelter organisms
(from both predators and physical disturbance) is often considered
one of the most important functions facilitating biodiversity (see
review by Boström et al., 2006), and in the absence of a meadow-
structure the positive effect of seagrasses on the benthic diversity
might be reduced. Finally, we expect the restored seagrass to
facilitate benthic biodiversity, but potentially to a lesser degree
than natural seagrasses, due the short time span after restoration.
With our findings we aim to explain the importance of intertidal
seagrass ecosystems for associated benthic communities and their
functionality, to evaluate seagrass restoration success beyond the
target species, and to provide practical recommendations
concerning the conservation and restoration of intertidal
seagrasses in the Wadden Sea and globally.
2 Methods
2.1 Study area
The Wadden Sea is a temperate coastal sea that extends from
the northwest Netherlands to the southwest coasts of Denmark. The
Wadden Sea has a diurnal tidal cycle (range: 1.5 to 4 meters) and
during low tide, approximately 50% of the seas total area (~8000
km²) emerges as intertidal flats. These tidal flats provide a hotspot
for birds and marine biodiversity.
2.2 Seagrass restoration
Since 2018, eelgrass (Z. marina) restoration trials have been
successfully performed northeast of Griend-island (Figure 1;
N 53.2692, E 5.2949) in the Dutch Wadden Sea (Gräfnings et al.,
2022;Gräfnings et al., 2023). Prior to restoration experiments in
2018, there was no eelgrass growing on the tidal flats surrounding
the island. In March 2020, a 400 m² plot was seeded on the Griend
sandflat with the DIS-method (Govers et al., 2022;Gräfnings et al.,
2022). In the restoration plot, eelgrass seeds were injected to a depth
of 3 cm, with ~3 seeds/injection and with a seeding density of 50
injections/m². In July 2020 on average 25.75 eelgrass plants/m² had
been established in the 400 m² restoration plot. A year later in July
2021, on average 25 second generation eelgrass plants/m² were
counted in the restoration plot.
2.3 Data collection and processing
In the summer (July–August) of 2018, 22 natural seagrass sites
were sampled once during low tide across the international Wadden
Sea (Figure 1). At each site, we estimated the % cover of Z. marina
and Z. noltii by walking three 30 m x 1 m belt transects. At 15 of the
sites, we collected samples both from inside and outside (>20 m
from the seagrass) of the seagrass. At the remaining 7 sites, samples
were only collected inside the seagrass. At each site, three benthic
macrofauna cores (top 30 cm & 15.5 cm diameter) were sampled.
Cores sampled from within the seagrass meadow always contained
seagrass. In the field, the samples were sieved (1 mm), after which
any seagrass biomass in the samples was separated and pooled.
Macrozoobenthos from the three cores were pooled and stored in
70% ethanol until identification. In July 2021, we sampled six
benthic macrofauna cores (top 30 cm & 15.5 cm diameter) inside
and outside the seagrass restoration plot at Griend (Figure 1E).
Samples were sieved (1 mm) and stored in a 4% formaldehyde
solution until identification. The twelve macrofauna cores from
Griend were treated as independent samples. In the lab, all
individuals were counted and identified to the finest taxonomic
level possible under a dissecting microscope. The individuals were
identified to 54 different taxonomic groups (35 at species-level, 11 at
genus-level (e.g., Eteone sp.), 2 at family-level (e.g., Polynoidae), 3 at
order-level (e.g., Actinaria), 2 at phylum-level (e.g., Nematoda) and
1 at class-level (Bivalvia). Once counted and identified, the biomass
of individuals of the same taxonomic group was determined per
sample. Samples were first dried for 48h at 60°C in a ventilated
stove, after which dry weight was measured. Following this, the
samples were incinerated for 5 hours at 560°C and then weighed
again to obtain the ash free dry mass (AFDM). Seagrass samples
were dried for 48 h at 60°C in a ventilated stove, after which the total
dry weight of the plants was measured.
2.4 Macrozoobenthos traits
We chose to include traits explaining the size, morphology,
mobility, feeding type, burrowing depth and reproduction of the
benthic communities (Table 1).Thesetraitswerechosento
characterize the basic ecology of the benthic animals and to give
an indication how intertidal seagrasses affect benthic ecosystem
functioning. All traits were categorical and divided into several
modalities (Table 1). The species-specificaffinities to all modalities
were fuzzy coded within a range from 0 to 3 (0= no affinity, 1= low
affinity, 2= moderate affinity and 3= high association of taxon with
the trait category). The fuzzy-coded trait values were extracted from
two macrozoobenthic biological trait databases (Gusmao et al.,
2022;Meijer et al., 2023). To standardize the data between traits
with different numbers of modalities, we divided the individual
modalities by the total number of modalities of the corresponding
trait (see Henseler et al., 2019). As we were not able to identify some
bivalves beyond class-level, these individuals were allocated trait
information common to the entire class in the Wadden Sea.
2.5 Statistical analysis
All statistical analyses were performed in R version 4.0.3 (R
Core Team, 2020). We investigated the effect of intertidal seagrasses
Gräfnings et al. 10.3389/fmars.2023.1294845
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on both taxonomic and functional diversity of macrozoobenthos.
To describe taxonomic diversity, we calculated taxonomic richness,
Shannon index and Pielou’s evenness using the “vegan”- package
(Oksanen et al., 2018). To describe functional diversity, we
calculated three trait-based indices (functional richness, evenness
and dispersion) corresponding to the previously mentioned
taxonomic indices. Functional richness (FRic) expresses the
amount of trait space that is occupied by the species of a
community (Mason et al., 2005). Functional evenness (FEve),
describes how evenly species abundances are distributed between
the expressed trait categories (Mason et al., 2005). Functional
dispersion (FDis) describes the abundance weighted mean
distance of individual species to their weighted group centroid in
the multidimensional trait space (Laliberteand Legendre, 2010)and
thus measures the spread of the community within the trait space.
Hence, functional dispersion can be considered a measure of
functional diversity (Laliberteand Legendre, 2010). Additionally,
community-level weighted means of trait values (CWM) were
computed for each sample. CWMs express trait values weighted
by species abundances and can be used to compare how
communities differ functionally. Functional diversity indices were
calculated with the “FD’’-package (Laliberteand Legendre, 2010;
Laliberteet al., 2014). We used count-data (individuals/m²) to
calculate the different indices and community-level weighted
means. Before calculating the trait-based indices, count-data was
log (x+1) transformed to reduce the influence of dominant species
without losing the abundance effect.
2.5.1 Analyzing the effect of natural intertidal
seagrass on benthic diversity
Differences in benthic diversity indices and abundances (counts
and AFDM) between natural seagrass and nearby bare areas were
analyzed with linear mixed effect models using the lmer-function in
R (package: “lme4”). In the models, we included data from sites
where macrozoobenthos was sampled both inside and outside the
seagrass (15 sites). No distinction between the two seagrass species
was included in these models. “Site”was included as a random
factor (random intercept: “1|Site”) in each model. Residuals of the
linear mixed effect models were checked for normality and, if
necessary,theresponsevariablewastransformedtofit model
assumptions (log-transformed: Taxonomic richness; sqrt-
transformed: FEve & FDis). An ANOVA from the car package
(Fox and Weisberg, 2011) was applied to conduct the Wald Chi-
Squared test on model outputs.
To investigate if the two seagrass species affect benthic
communities differently in the intertidal Wadden Sea, we first
divided the sampled seagrass meadows into three categories: Mixed
meadows (both seagrass species present; n=5), monospecificZ.
marina (n=8) and monospecificZ. noltii (n=9). Data from all
sampled seagrass sites (22 sites) were used for the analyses. One-
way ANOVAs were performed to analyze if benthic diversity indices
differed between seagrass meadow types, after controlling that the
data met the assumptions of parametric tests. Additionally, linear
regressions were performed to investigate if seagrass cover (%) and
biomass (DW, g) affected benthic diversity indices.
FIGURE 1
(A) Location of the Wadden Sea in Europe. (B) Locations of sampled seagrass sites in the Wadden Sea where green indicates sites macrozoobenthos
was sampled both inside and outside the seagrass and yellow indicates sites macrozoobenthos was sampled only inside the seagrass. The red circle
indicates the seagrass restoration site northeast of Griend-island. Pictures on the right show (C) a mixed Zostera noltii &Zostera marina meadow, (D)
a monospecificZ. marina meadow and (E) the restoration plot at Griend.
Gräfnings et al. 10.3389/fmars.2023.1294845
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2.5.2 Analyzing the effect of restored intertidal
seagrass on benthic diversity
Differences in benthic diversity indices (taxonomic richness,
Shannon index, Pielou’s evenness FRic, FEve, FDis) and
abundances (counts and AFDM) between the restored seagrass
plot at Griend (n=6) and nearby bare area (n=6) was analyzed with
one-way ANOVAs. Prior to analysis, data were tested to meet the
assumptions of parametric tests.
2.5.3 Analyzing the effect of intertidal seagrass on
benthic community composition
To assess if benthic communities differed between seagrasses
and nearby bare areas, we performed non-metric multidimensional
scaling (nMDS) on the taxonomic (based on counts) and functional
(based on CWM values) compositions. The replicates from the
seagrass restoration site were pooled (seagrass and bare separately)
and included in the analysis, to get an indication if restored seagrass
affected benthic communities similarly as natural meadows. Bray-
Curtis dissimilarity was applied for count-data and the Gower
distance for CWM trait values. To statistically test for differences
in taxonomic and functional compositions among habitats, we used
permutational multivariate ANOVAs (PERMANOVA;9999
permutations; package: “vegan”). Site was included as a random
factor in the PERMANOVA analysis. Before PERMANOVAs were
performed, we checked with a permutational test of multivariate
dispersion (PERMDISP; package: “vegan”) if the observations
within groups were spread equally between the habitats.
Furthermore, we used Multilevel pattern analysis (package:
“indicspecies”) to determine which species and modalities were
driving differences between seagrass and bare communities.
Multilevel pattern analysis was performed separately for natural
meadows (n=15) and the restoration site (n=6).
3 Results
3.1 Effect of (natural) intertidal seagrass on
benthic diversity
Benthic taxonomic richness was significantly increased by
natural intertidal seagrasses (chi²=7.47, df=1, p=0.006), with
seagrasses sheltering on average 33% higher taxonomic richness
TABLE 1 List of macrozoobenthos traits and their modalities used in
functional trait analysis.
Trait Modality Label Relevance
Bioturbation
type
Epifauna E Habitat modification, sediment
processing, nutrient cycling
Surficial
modifier
SM
Upward
conveyor
UC
Downward
conveyor
DC
Bio diffuser BD
Regenerator Re
Burrowing
depth, cm
Surface Su Space usage, bioturbation
0-3 0-3
3-8 3-8
8-15 8-15
15-25 15-25
>25 >25
Adult body
size, mm
<5 5 Productivity, palatability
5-10 5-10
10-20 10-20
20-40 20-40
40-80 40-80
80-160 80-160
>160 >160
Feeding
mode
Deposit
feeder
DF Food acquisition, trophic level
Suspension
feeder
SF
Scavenger/
Opportunistic
OS
Grazer G
Predator P
Longevity,
years
<1 1 Life span, productivity
1-3 1-3
3-6 3-6
6-10 6-10
>10 >10
Adult
movement
type
Sessile Se Mobility, dispersal, ability to
escape predation
Swimmer/
Floater
S/F
Crawler/
Walker
C/W
Burrowing Bu
Reproduction Asexual A Reproduction, productivity
(Continued)
TABLE 1 Continued
Trait Modality Label Relevance
Broadcast Bc
Brooder/
Egg layer
Br
Benthic Be
Skeleton Soft So Palatability
Calcified Ca
Chitinous Ch
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than nearby bare areas (Figure 2A). The presence of seagrass on
average doubled the amount of epifaunal richness (chi²=13.26,
df=1, p<0.001), while no significant differences were observed in
endobenthic taxonomic richness (Supplementary Figure S1).
However, interestingly seagrass presence did not significantly
affect either Pielou’s evenness or Shannon index (Figures 2C,E).
The patterns in functional diversity indices largely mirrored
their taxonomic counterparts. Functional richness was significantly
higher in the presence of intertidal seagrasses (chi²=6.17, df=1,
p=0.013; Figure 2B), signifying that the number of expressed traits
was increased by seagrass presence. However, neither functional
evenness or dispersion of benthic communities differed significantly
between seagrasses and bare areas (Figures 2D,F). On average,
170% more benthic individuals inhabited seagrasses than nearby
bare areas (chi²=4.87, df=1, p=0.027, Figure 3A), while the animals’
biomass did not differ significantly between the habitats (Figure 3B).
No significant differences were found in macrozoobenthic diversity
indices between the three seagrass categories (Mixed meadows,
monospecificZ. marina and monospecificZ. noltii;Figure 4).
Additionally, no correlation was found between site-wide seagrass
cover % and benthic diversity indices (both taxonomic and
functional; Supplementary Figures S2A,C,E,G,I,K). Similarly, no
correlation was discovered between seagrass biomass (dry weight, g)
and benthic diversity indices (both taxonomic and functional;
Supplementary Figures S2B,D,F,H,J,L).
3.2 Effect of restored intertidal seagrass on
benthic diversity
The recently restored Z. marina meadow at Griend (<2 years) had
an almost identical effect on benthic taxonomic diversity as naturally
occurring seagrasses in the Wadden Sea. Benthic taxonomic richness
was 32% higher in the restored seagrass meadow compared to nearby
bare area (F(1,10) = 8.76, p= 0.014; Figure 2A). Similar to natural
meadows, the restored seagrass did not affect either Pielou’sevenness
or Shannon index significantly (Figures 2C,E). Additionally, the
patterns in functional diversity indices largely mirrored their
B
CD
EF
A
FIGURE 2
Taxonomic and trait-based indices inside and outside seagrass in natural meadows and in the restored meadow: (A) Taxonomic richness (B)
Functional richness, (C) Pielou’s evenness, (D) Functional evenness, (E) Shannon index and (F) Functional dispersion. Boxplots show median (line in
box), upper and lower quartile (box), 1.5 x interquartile range (vertical line) and outliers (circle). The indices were calculated with count-data
(indviduals/m²). Stars indicate significance of p<0.001 for ***, p<0.01 for ** and p<0.05 for *. Statistically non-significant results are indicated with ns.
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taxonomic counterparts. Similar to natural meadows, functional
richness was also higher in the restoration plot compared to nearby
bare area (F(1,10) = 13.23, p=0.004;Figure 2B), signifying that the
amount of expressed traits in the benthic community was increased
through seagrass restoration. However, unlike in the natural meadows,
the restored seagrass also significantly increased functional dispersion
of the macrozoobenthos (F(1,10) = 22.23, p< 0.001; Figure 2F),
signifying that the diversity of expressed traits was higher in the
restoration plots compared to the nearby bare area. Functional
evenness of the associated benthic communities did not significantly
differ in the restoration plot and nearby bare area (Figure 2D). In
contrast to natural seagrasses, we found no difference in animal counts
between the restored seagrass and nearby bare area (Figure 3A), while
biomass of the benthic community was almost 3x higher in the restored
seagrass (F(1,10) = 20.12, p= 0.001; Figure 3B). Mainly three benthic
species (mudsnail Peringia ulvae,commoncockleCerastoderma edule
and ragworm Hediste diversicolor) were responsible for the higher
biomass measured in the restored seagrass.
3.3 Effect of intertidal seagrass on benthic
community composition
Benthic community composition was significantly different in
the presence of seagrass compared to nearby bare areas (Figure 5),
both taxonomically (PERMANOVA; p= 0.04) and functionally (p=
0.001). Interestingly, the restored seagrass meadow seemed to affect
the benthic community similarly as natural meadows (Figure 5).
Blue mussels (Mytilus edulis), isopods (Idotea spp.) and juvenile
shore crabs (Carcinus maenas) functioned as indicator species for
seagrass meadows in the Wadden Sea (Multilevel pattern analysis,
p<0.05). At the restoration site, blue mussels (Mytilus edulis),
mudsnails (Peringia ulvae), nematodes and ragworms (Hediste
diversicolor) were indicative of benthic communities in the
seagrass, while two polychaeta species (Notomastus latericeus &
Heteromastus filiformis) functioned as indicator species for the bare
area. Many trait modalities were driving the differences in
functional composition between benthic communities in seagrass
and bare sites, both on the Wadden Sea scale and at the restoration
site (Figure 6). Trait modalities linked to epifaunal species (e.g.,
sessile, surface living and suspension feeding) were expressed more
in seagrass, while the most significant trait modalities telling bare
areas apart from seagrasses were: burrowing movement type,
deposit feeding and soft skeleton (Figure 6).
4 Discussion
Our results show that seagrasses (Zostera marina and Zostera
noltii) increase the richness of benthic diversity in the intertidal
Wadden Sea. By facilitating epifaunal animals, seagrasses support
distinct benthic communities that differ from unvegetated areas
both taxonomically and functionally. Importantly, we found that
seagrass restoration can quickly (within 2 years) facilitate benthic
communities to be taxonomically and functionally similar to
communities found in natural seagrass meadows. Hence, we show
that the current intertidal seagrass restoration practice in the Dutch
Wadden Sea not only leads to restored plants, but also aids in the
B
A
FIGURE 3
(A) Counts of individuals and (B) AFDM of macrozoobenthos inside and outside seagrass in natural meadows and at the restoration site. Boxplots
show median (line in box), upper and lower quartile (box), 1.5 x interquartile range (vertical line) and outliers (circle). Stars indicate significance of
p<0.01 for ** and p<0.05 for *. Statistically non-significant results are indicated with ns.
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FIGURE 5
nMDS on taxonomic composition based on count-data and functional composition based on CWM values. Green circles indicate seagrass, orange
triangles bare areas and the blue color indicates the two data points of the restoration site. Lines between points signify that data belongs to the
same site.
B
CD
EF
A
FIGURE 4
Taxonomic and trait-based indices of different seagrass meadow types [Mixed meadow (both seagrass species present; n=5), monospecificZ. marina
(n=8) and monospecificZ. noltii (n=9)] in the Wadden Sea: (A) Taxonomic richness (B) Functional richness, (C) Pielou’s evenness, (D) Functional
evenness, (E) Shannon index and (F) Functional dispersion. Boxplots show median (line in box), upper and lower quartile (box), 1.5 x interquartile
range (vertical line) and outliers (circle). The indices were calculated with count-data (indviduals/m²). No statistical differences were detected.
Gräfnings et al. 10.3389/fmars.2023.1294845
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regeneration of ecosystem integrity through enhancing both
taxonomic and functional diversity.
4.1 Intertidal seagrass enhances benthic
biodiversity in the Wadden Sea
The effect of seagrasses on biodiversity is well studied and
literature shows that the presence of seagrass usually increases the
diversity and abundance of benthic fauna (e.g., Orth et al., 1984;
Boström et al., 2006). We found that in the intertidal Wadden Sea,
seagrasses also support richer (both taxonomically and
functionally) and more abundant benthic communities. However,
benthic taxonomic richness in the Wadden Sea was lower than what
is generally measured in Atlantic seagrass meadows (species
richness varying between 10-60; Orth, 1973;Stoner, 1980;Edgar
et al., 1994;Blanchet et al., 2004 and references within). This may be
the result of challenging living conditions that animals are subjected
to in the intertidal Wadden Sea. Seagrasses in the Wadden Sea grow
in the upper intertidal zone, which means that the plants and
associated communities emerge over the water level for several
hours (>5h) each tidal cycle. For most marine species, emergence
(even short periods) is very stressful (increased desiccation/
temperature) and thus only specialized or resistant benthic
species inhabit the area. The ability of seagrasses to modify and
ameliorate local conditions is crucial to support rich benthic life in
seagrass systems. For instance, the ability of seagrass meadows to
provide animals shelter, stabilize sediments, reduce hydrodynamics,
aerate sediments and recycle nutrients, are all processes that change
living conditions on the bottom of the sea and facilitate
macrozoobenthos (Orth et al., 1984;Boström et al., 2006;van der
Zee et al., 2016). In the intertidal Wadden Sea, we suggest that
seagrasses facilitated species richness by providing shelter (from
predators/hydrodynamics/desiccation), food-provisioning and
attachment structures to benthic animals.
Interestingly, intertidal seagrasses affected benthic diversity and
community compositions very similarly across the Wadden Sea,
despite the large spatial scale and differences in seagrass species
composition. Worth highlighting is the fact that seagrass presence
affected functional compositions more uniformly than their
taxonomic counterparts (Figure 5), which suggests that seagrasses
facilitate certain traits rather than specific macrozoobenthic species.
Functional diversity, and more broadly ecosystem function, is then
driven by density shifts in trait representation rather than the
presence or absence of traits (e.g., Hewitt et al., 2008).
Additionally, we found that higher seagrass cover % and biomass
had no detectable influence on benthic diversity. This is somewhat
surprising, as the ability of seagrasses to form meadows and modify
their environment has previously often been linked with higher
benthic richness (Boström et al., 2006 and references within). In our
study, monospecificZ. marina meadows with very low cover % (< 1
plant/m²) supported similar benthic communities as dense
perennial Z. noltii meadows. Hence our results suggest that the
mere presence of seagrass, regardless of species or meadow
structure, seems to facilitate benthic biodiversity in the intertidal
Wadden Sea. However, seagrasses in the intertidal Wadden Sea
FIGURE 6
Mean CWM values for benthic communities at seagrass meadows and nearby bare areas in the Wadden Sea and at the restoration site. The stars
indicate significant results of the Multilevel pattern analysis highlighting which modalities indicate either seagrass or bare areas. Stars stand for
p<0.001 for ***, p<0.01 for ** and p<0.05 for *. For label descriptions, see Table 1.
Gräfnings et al. 10.3389/fmars.2023.1294845
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provide benthic animals only seasonal hotspots, as during the
winter period most aboveground biomass is lost. Thus, benthic
communities or at least epifauna need to recolonize the beds each
spring. Interestingly, the only benthic species that was exclusively
found in samples taken inside the seagrass meadows, was the
economically and ecologically important blue mussel (Mytilus
edulis). Thus, our results suggest that seagrasses can potentially
provide a stepping stone/refuge for mussel spat, facilitating the
dispersal of these valuable bivalves.
4.2 Seagrass restoration quickly facilitates
benthic communities
Ecological restoration generally aims at restoring ecological
integrity by regenerating high biodiversity and lost ecosystem
functions. Here, after only two growing seasons a relatively small-
scale restoration plot facilitated similar benthic diversity as natural
meadows in the Wadden Sea. Our results are especially promising
when considering that aquatic restoration efforts often fail to
introduce diversity of associated communities to pre-disturbance
levels (Rey Benayas et al., 2009). Successful recovery of diversity has
most often been observed in systems that are dominated by fast-
reproducing organisms with high dispersal ability (Jones and
Schmitz, 2009;Duarte et al., 2015). This is most likely also the
case in the Wadden Sea, where natural meadows need to be
recolonized each spring by epifaunal animals (as discussed
above), and one of the main reasons why diversity was able to
rebound so quickly at the restoration site. Additionally, most
benthic species in this study were found both in seagrass and on
the adjacent bare flats, which suggests that intertidal seagrasses do
not shelter unique species, but instead provide larger niche spaces
withroomforricheraggregations. Presumably, mainly by
providing aboveground structure and protection, seagrasses
facilitate epifaunal animals and traits associated with life above
the sediment surface (e.g., sessile, surface living, suspension feeder,
Figure 6). Importantly, by investigating the facilitated traits and
overall functional diversity of the benthic communities, we could
establish that the restored seagrass meadow also functioned very
similarly to natural meadows. When comparing restoration efforts
over large geographical scales, variation in species assemblages can
obscure restoration success, whereas functional trait assemblages
may provide a more general indicator of restoration success as they
remain more stable over large distances (Bremner, 2008;Hewitt
et al., 2008). We concur with previous studies (Dolbeth et al., 2013;
Lefcheck et al., 2017) highlighting the usefulness of functional
diversity measurements as predictors for seagrass restoration
success and urge future restoration projects to incorporate this
approach when evaluating restoration success.
4.3 Study limitations
It is important to note the limitations of the study. We only
investigated one restoration site, restored with only one of the two
native seagrass species and therefore the results of this study cannot be
generalized. However, as the included restoration site is the only site
where seagrass restoration has been performed successfully in the
whole Wadden Sea, we argue that this study should be seen as an
important early indication of the value and potential of intertidal
seagrass restoration in this area. Additionally, we only investigated the
effect of seagrasses on benthic diversity and therefore further research is
needed to investigate how the restoration of intertidal seagrass may
affect higher trophic levels such as fish and birds. We expect that
intertidal seagrasses can also indirectly benefit higher trophic levels
(birds and fish) by increasing food availability. For instance, it has been
shown that fish diversity is positively influenced by benthic species
richness (Lebreton et al., 2012). In light of our results, we expect that
especially predators of epifaunal species (e.g., sanderling Calidris alba)
and herbivorous birds (e.g., brent geese Branta bernicla) can benefit
from seagrass presence in the intertidal Wadden Sea.
4.4 Implications for seagrass conservation
and restoration
Our results have important implications for the future of seagrass
restoration in the intertidal Wadden Sea. We show that active
restoration resulted in the recovery of a threatened marine habitat
(intertidal seagrass), restoration of biodiversity and provisioning of
habitat. Tangible deliverables like these, can be used to effectively
engage stakeholders and to communicate the value of intertidal
seagrasses and that restoration of these valuable habitats is possible.
Additionally, we argue that dwarf eelgrass (Z. noltii) should be better
incorporated in future restoration efforts in the Wadden Sea, as our
results show that the smaller seagrass increases benthic diversity to a
similar degree as Z. marina. Thus far restoration efforts in the Dutch
Wadden Sea have primarily targeted Z. marina, but considering our
results we argue that Z. noltii should also get a more visible role in
conservation and restoration practices, due to the species ecological
importance and ability to create stable perennial meadows.
Data availability statement
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation.
Ethics statement
The manuscript presents research on animals that do not
require ethical approval for their study.
Author contributions
MG: Conceptualization, Formal analysis, Investigation,
Visualization, Writing –original draft, Writing –review &
editing. IG: Formal analysis, Investigation, Writing –review &
editing. SV: Investigation, Writing –review & editing. IF:
Investigation, Writing –review & editing. TV: Conceptualization,
Gräfnings et al. 10.3389/fmars.2023.1294845
Frontiers in Marine Science frontiersin.org10

Funding acquisition, Supervision, Writing –review & editing. JH:
Conceptualization, Investigation, Writing –review & editing,
Funding acquisition. KM: Resources, Writing –review & editing.
BE: Resources, Writing –review & editing. QS: Funding acquisition,
Writing –review & editing. LG: Conceptualization, Funding
acquisition, Investigation, Supervision, Writing –review & editing.
Funding
The author(s) declare financial support was received for the
research, authorship, and/or publication of this article. This project
was funded by Waddenfonds grant ‘Sleutelen aan zeegrasherstel’
and European Union’s Horizon 2020 research and innovation
program (project: MERCES, Marine Ecosystem Restoration in
Changing European Seas; grant agreement #689518).
Acknowledgments
We acknowledge the benthos-lab of NIOZ and especially Loran
Kleine Schaars for their help with macrozoobenthos identification.
Lisa Bruil is acknowledged for her help in the field. We would like to
thank the reviewers for their helpful comments that improved
this manuscript.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
The author(s) declared that they were an editorial board
member of Frontiers, at the time of submission. This had no
impact on the peer review process and the final decision.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online
at: https://www.frontiersin.org/articles/10.3389/fmars.2023.1294845/
full#supplementary-material
SUPPLEMENTARY FIGURE 1
Epi- and endobenthic taxonomic richness inside and outside natural seagrass
meadows and the restored meadow. Boxplots show median (line in box),
upper and lower quartile (box), 1.5 x interquartile range (vertical line) and
outliers (circle). Stars indicate significance of p<0.001 for ***, p<0.01 for **
and p<0.05 for *.
SUPPLEMENTARY FIGURE 2
Relationships between seagrass cover % and benthic (A) taxonomic richness,
(C) functional richness, (E) Pielou’s evenness, (G) Functional evenness, (I)
Shannon index and (K) Functional dispersion in the intertidal Wadden Sea.
Relationships between seagrass dry weight (g) and benthic (B) taxonomic
richness (D) functional richness, (F) Pielou’s evenness, (H) Functional
evenness, (J) Shannon index and (L) Functional dispersion in the intertidal
Wadden Sea.
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