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Trophic structure and resource utilization of the coastal fish community in the western Wadden Sea: evidence from stable isotope data analysis

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Trophic structure and resource utilization of the coastal fish community in the western Wadden Sea: evidence from stable isotope data analysis

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We studied the trophic structure of the western Wadden Sea fish community through stable isotope analysis (δ13C and δ15N) of 1658 samples from 57 fish species collected between 2012 and 2016. Stable isotope values differed between species but did not vary between years or seasons, and only for some species with fish size. Stable isotope values were not different between immigrating (spring) and emigrating (autumn) fish, suggesting a similar trophic niche of the various fish species in the coastal zone and inside the Wadden Sea. For the majority of species, average δ13C values were within the range of −12 to −20.5‰, showing that both (marine) pelagic and benthic primary producers were at the base of the food web. Average δ15N values varied among species from 13−18‰, resulting in estimated trophic positions (TPs) of 2.1−5.5 with the majority between 2.2 and 3.5. Thick-lipped grey mullet Chelon labrosus, golden grey mullet C. aurata, greater pipefish Syngnathus acus and pilchard Sardina pilchardus had the lowest TP (2.2−2.4). Among the common species (>10 observations), the highest TP values (3.4−3.5) were found for twaite shad Alosa fallax, smelt Osmerus eperlanus, bull-rout Myoxocephalus scorpius, bass Dicentrarchus labrax and cod Gadus morhua. For all species, estimated TPs based on isotope values were lower than those based on stomach content composition (2.0−4.7), which could be explained by species-specific differences in trophic fractionation or by underestimation of the contribution of smaller prey species in the stomach content analysis. The trophic niche space of benthopelagic species was the smallest and overlapped with that of the pelagic and benthic species. In terms of area use, trophic niche space was smaller for juvenile marine migrant species (nursery-type species) and overlapped with that of the (near-)resident species and marine seasonal visitors. Potentially, trophic competition is highest for the functional group of benthopelagic species and the guild of juvenile marine migrant species (nursery-type species).
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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 677: 115–128, 2021
https://doi.org/10.3354/meps13855 Published October 28
1. INTRODUCTION
Shallow coastal systems are often highly produc-
tive areas due to the import of nutrients and organic
matter from river runoff and the open sea (Nixon
1995, Cloern et al. 2014). As a consequence, these
areas are important foraging grounds for a variety of
fish, bird and marine mammal species (e.g. Goodall
© Inter-Research 2021 · www.int-res.com*Corresponding author: suzanne.poiesz@nioz.nl
Trophic structure and resource utilization of the
coastal fish community in the western Wadden Sea:
evidence from stable isotope data analysis
Suzanne S. H. Poiesz1,2,*, Johannes IJ. Witte1, Marcel T. J. van der Meer3,
Henk W. van der Veer1, Karline E. R. Soetaert4
1NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, PO Box 59, 1790 AB, Den Burg, Texel,
The Netherlands
2Faculty of Science and Engineering, Groningen Institute of Evolutionary Life Sciences, University of Groningen,
PO Box 11103, 9700 CC Groningen, The Netherlands
3NIOZ Royal Netherlands Institute for Sea Research, Department of Microbiology and Biogeochemistry, PO Box 59, 1790 AB,
Den Burg, Texel, The Netherlands
4NIOZ Royal Netherlands Institute for Sea Research, Department of Estuarine and Delta Systems, PO Box 140, 4400 AC,
Yerseke, The Netherlands
ABSTRACT: We studied the trophic structure of the western Wadden Sea fish community through
stable isotope analysis (δ13C and δ15N) of 1658 samples from 57 fish species collected between
2012 and 2016. Stable isotope values differed between species but did not vary between years or
seasons, and only for some species with fish size. Stable isotope values were not different between
immigrating (spring) and emigrating (autumn) fish, suggesting a similar trophic niche of the vari-
ous fish species in the coastal zone and inside the Wadden Sea. For the majority of species, aver-
age δ13C values were within the range of −12 to −20.5‰, showing that both (marine) pelagic and
benthic primary producers were at the base of the food web. Average δ15N values varied among
species from 13−18‰, resulting in estimated trophic positions (TPs) of 2.1−5.5 with the majority
between 2.2 and 3.5. Thick-lipped grey mullet Chelon labrosus, golden grey mullet C. aurata,
greater pipefish Syngnathus acus and pilchard Sardina pilchardus had the lowest TP (2.2−2.4).
Among the common species (>10 observations), the highest TP values (3.4−3.5) were found for
twaite shad Alosa fallax, smelt Osmerus eperlanus, bull-rout Myoxocephalus scorpius, bass Di cen -
trarchus labrax and cod Gadus morhua. For all species, estimated TPs based on isotope values
were lower than those based on stomach content composition (2.0−4.7), which could be explained
by species-specific differences in trophic fractionation or by underestimation of the contribution of
smaller prey species in the stomach content analysis. The trophic niche space of benthopelagic
species was the smallest and overlapped with that of the pelagic and benthic species. In terms of
area use, trophic niche space was smaller for juvenile marine migrant species (nursery-type spe-
cies) and overlapped with that of the (near-)resident species and marine seasonal visitors. Poten-
tially, trophic competition is highest for the functional group of benthopelagic species and the
guild of juvenile marine migrant species (nursery-type species).
KEY WORDS: Coastal fish community · Wadden Sea · Stable isotopes · Trophic position ·
Trophic structure
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Mar Ecol Prog Ser 677: 115–128, 2021
1983). Worldwide, these coastal areas have been under
anthropogenic threat for centuries, which has caused
major disturbance and structural and functional
changes to the systems (see for instance Jackson et
al. 2001, Lotze et al. 2005, 2006). In the future, threats
such as overfishing, climate change (e.g. warming,
acidification, deoxygenation), habitat de struction and
pollution are expected to increase (Bijma et al. 2013,
European Marine Board 2013). Predicting the conse-
quences of these threats on the future productivity of
coastal areas requires (among other factors) insight
into the food web structure of these systems.
Historically, food web studies have been, and still
are, based on taxonomic identification of prey items
via stomach content analysis (Hynes 1950). The
strength of stomach content analysis is that it pro-
vides detailed information about predator−prey re -
lationships. However, its limitations are that only vis-
ible larger prey items can be identified, it offers only
a small snapshot in time of recent prey items and it
requires extensive taxonomic knowledge. Stable iso-
tope measurements (Minagawa & Wada 1984) over-
came the snapshot problem by providing a more
integrated signal of assimilated prey over a longer
time period. Stable nitrogen isotope values (δ15N)
increase with trophic position (TP) (Minagawa &
Wada 1984). Carbon isotope (δ13C) values are an in -
dication of different carbon sources (Hecky & Hess -
lein 1995), provided that these have significantly dif-
ferent values. Therefore, δ13C and δ15N have been
increasingly used as indicators of both habitat use
and TP (Post 2002, McCutchan et al. 2003, Boecklen
et al. 2011, Abrantes et al. 2014, Christianen et al.
2017), while insight into predator−prey relationships
still relies on taxonomic identification of prey items
via stomach content analysis. Food web structure
analysis benefits most from a combination of both
stomach content and stable isotope analysis. By com-
bining these 2 types of analyses, complementary
results of the food web structure and food web func-
tioning and dynamics can be obtained (Preciado et
al. 2017, Park et al. 2018, Bissattini et al. 2021).
One of the most important European temperate
coastal areas is the Wadden Sea, an estuarine area
bordering the Dutch, German and Danish coast. It is
recognized as an important nursery area for a variety
of fish species (Zijlstra 1972) and a resting and feed-
ing area for wading birds (Wol 1983). For the Wad-
den Sea, food web studies started with static carbon
flow models of the intertidal (Kuipers et al. 1981) and
subtidal (de Wilde & Beukema 1984). Later, spatial
and temporal fluctuations were investigated using
ecological network analysis (ENA) (Baird et al. 2011,
2012, Schückel et al. 2015, de Jonge et al. 2019a,b,
Jung et al. 2020) and dynamic energy flow budget
models (Baretta & Ruardij 1988, Lindeboom et al.
1989). Recently, some aspects of the Wadden Sea
food web have been studied using stable isotopes.
From an extensive sampling campaign in the Dutch
Wadden Sea, Christianen et al. (2017) concluded that
the benthic primary producers (micro-phytobenthos)
were the most important energy source for the major-
ity of consumers at higher TPs in late summer but, in
line with Deegan & Garritt (1997), large spatial het-
erogeneity was observed. Jung et al. (2019) pointed
out that the Wadden Sea food web also showed sea-
sonal variability, highlighting the important role of
freshwater energy inputs. Both studies mainly focussed
on the macrobenthic community, and al though these
studies included some information about fish, de -
tailed stable isotope analysis of the TP of the Wadden
Sea fish community is still lacking.
So far, trophic food web structure of the Wadden
Sea fish community, including predator−prey rela-
tionships, has only been analysed in detail based on
stomach content information in the Sylt-Rømø Bight
basin (Kellnreitner et al. 2012) and the Marsdiep
basin (Poiesz et al. 2020). In this study, the food web
structure of the fish community of the Marsdiep
basin in the western Dutch Wadden Sea was ana-
lysed based on stable isotopes combined with infor-
mation about primary producers in the area (Chris-
tianen et al. 2017). Calculated TPs were compared
with estimates based on dietary information from
stomach content data (Poiesz et al. 2020). Further-
more, for all species, the size of the trophic niche
was determined. These trophic niches comprise all
trophic inter actions that connect a species to others
in the eco system (Elton 1927) and represents a
species’ overall trophic role (Leibold 1995). In addi-
tion, niche overlap within fish communities indicates
potential trophic competition among different
groups (Dubois & Co lombo 2014). Previous analysis
of trophic structure based on stomach content infor-
mation (Poiesz et al. 2020) showed a pivotal position
of a few key prey species, namely amphipods,
brown shrimps, juvenile herring and gobies. To link
the present study with Poiesz et al. (2020), the
stable isotope values of these key prey species were
also determined. Furthermore, the trophic niches of
the individual fish species were determined in rela-
tion to their use of the area as a (near-)resident spe-
cies, juvenile marine migrant or marine seasonal
visitor as well as in relation to their feeding type
(benthic, benthopelagic, pelagic), following Zijlstra
(1983) and Elliott & Dewailly (1995).
116
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Poiesz et al.: Wadden Sea fish community explained through stable isotopes
2. MATERIALS AND METHODS
2.1. Sampling
From 2012−2016, fish were collected from the cat -
ches of a long-term monitoring programme of fish
fauna, using a passive fish trap near the entrance of
the Wadden Sea (Fig. 1). This kom-fyke, with a
stretched mesh-size of 20 mm, consisted of a leader
of 200 m running from the beach towards deeper
waters. Fish swimming against the leader are guided
towards 2 chambers (the so-called ‘kom’) and from
there, collected into the kom-fyke. Fishing took place
in spring (April, May, June) and autumn (September,
October), and during this period the kom-fyke was
emptied every day whenever weather conditions
permitted. During the winter and summer months,
the kom-fyke was removed due to the risk of po -
tential damage by ice in winter and extreme algal
blooms and high numbers of jellyfish during summer.
For more information, see van der Veer et al. (2015).
Key prey species according to Poiesz et al. (2020)
were collected nearby the kom-fyke by means of
fine-meshed pelagic and demersal trawls.
All fish and prey species that were caught were
taken back to the laboratory, sorted immediately,
identified to species level, counted, measured and
weighed. Occasionally, fish would be damaged by
shore crabs and their exact weight could not be de -
termined. A maximum of 3 individuals per fish spe-
cies per week, preferably of different sizes, were
selected and stored at −20°C for dissection. Within a
few weeks of storage, fish were defrosted and
thawed, and isotope samples (dorsal muscle tissue
directly posterior to the head) were taken in line with
Svensson et al. (2014), placed in a 1.5 ml centrifuge
vial and stored at −80°C. After freeze-drying for 48 h,
the isotope samples were ground and homogenized.
Next, 2 samples of 0.4−0.8 mg were weighed and
folded into small tin cups for analysis. The δ15N, δ13C,
% total organic carbon (%TOC) and % total nitrogen
(%TN) contents were measured at the Royal Nether-
lands Institute for Sea Research (NIOZ) with a
Thermo Scientific Delta V Advantage Isotope Mass
Spectrometer linked with a Flash 2000 Organic Ele-
ment Analyzer. During each sample run, monitoring
gas (N2and CO2) with a predetermined isotopic com-
position was used to determine the δvalues of both
the samples and the standards.
Standards with known isotopic composition were
weighed and included on each plate of 94 spots
(Acetanilide, Urea and Casein) at the beginning of
the analysis, after every 12 samples and at the end of
each sequence in order to monitor the process of
measuring and correct for the offset between the
measured and actual isotope ratio. One standard,
Acetanilide, was used to correct the measured values
and the other 2 standards, Urea and Casein, to check
the correction. Analytical reproducibility was 0.3
for δ15N and 0.1‰ for δ13C throughout every se -
quence. Before the standards, each sequence started
with multiple blanks (empty tin cups) to remove air if
present and to determine a potential blank contribu-
tion to the analysis. Blanks were typically too low to
be of any importance.
Isotope value of the sample (δX) was expressed as
a ratio, in delta (δ) notation in per mil (‰), relative to
an internationally defined reference:
(1)
where Rsample and Rreference are the ratio between the
‘heavy’ and ‘light’ isotopes (15N:14N or 13C:12C) of the
/ – 1 1000
sample reference
()
XR R
117
Fig. 1. Sampling location of the Royal Netherlands Institute
for Sea Research (NIOZ) kom-fyke near the island of Texel.
Top panel: western Dutch Wadden Sea (black box); red
arrow: inwards migration in spring; blue arrow: outward
migration in autumn. Lower panel: kom-fyke position (black
bar). Grey: intertidal areas (after Poiesz et al. 2020)
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Mar Ecol Prog Ser 677: 115–128, 2021
sample and the reference, respectively. The δ15N val-
ues are reported against atmospheric N and δ13C
against Vienna Peedee-Belemnite (VPDB). All infor-
mation was added to a database.
2.2. Stable isotopes
The δ13C values were corrected for lipid content
according to Svensson et al. (2014):
(2)
where δ13Ccorr is the calculated δ13C value corrected
for lipid content, δ13Cbulk is the δ13C value of the bulk
tissue (δ13C values including lipid content) and C:N is
the ratio of %TN / %TOC. These lipid-content-
corrected δ13C values were used in all further analyses.
Isotopic values of δ15N and δ13C were analysed in
relation to fish length and season for species with 57
or more isotopic measurements. Linear relationships
were calculated by fitting a model according to:
δ13C = β1× fish species + factor (season)
+ fish length (cm) (3)
and
δ15N = β1× fish species + factor (season)
+ fish length (cm) (4)
where β1is the slope indicating the change of δ15N/
δ13C on average when factor (season) and/or length
(cm) increases one unit; and where season refers to
spring or autumn sampling.
2.3. Trophic position
Feeding niches of the fish species were analysed,
distinguishing between their guilds and functional
groups. The guild represents how a species uses the
area (Wadden Sea) as a (near-)resident species (NR),
juvenile marine migrant (JMM) or marine seasonal
visitor (MSV) following Zijlstra (1983). Species were
also classified into 3 functional groups (benthic,
bentho pelagic and pelagic) based on habitat position
(e.g. bottom-dwelling, near the bottom or swimming
in the water column) and method of food acquisition
(Dumay et al. 2004).
TPs for each fish species were estimated according
to a dual baseline Bayesian approach, which in -
cludes a mixing model to discriminate among 2 dis-
tinct sources of C and N, e.g. pelagic vs. benthic
baselines (van der Zanden et al. 1997, Post 2002), in
line with Christianen et al. (2017). To perform the
Bayesian analysis, the first step was based on one
baseline with the trophic fractionation factor for N
only:
(5)
where δ15Ncis the δ15N value of the consumer, δ15Nb
is the δ15N value of the single baseline, ΔN is the
trophic fractionation factor for N, TP is the trophic
position of the consumer and λis the trophic position
of the baseline.
In order to extend this analysis to 2 baselines
(pelagic and benthic) with 2 distinct sources (N and
C), the formula for N becomes:
(6)
where δ15Nb1, δ15Nb2 are the δ15N values of baselines
1 and 2, respectively and αis the proportion of N
derived from baseline 1 (van der Zanden et al. 1997,
Post 2002).
The full model of 2 baselines for C is rewritten to
derive α:
(7)
where δ13Cb1, δ13Cb2 are the δ13C values of baselines
1 and 2, respectively, δ13Ccis the δ13C of the con-
sumer and ΔC the trophic fractionation factor for
carbon.
Freshwater and estuarine suspended particulate
organic matter values for the Marsdiep area were
taken from Jung et al. (2019). Data on pelagic and
benthic baselines were taken from Christianen et al.
(2017). In line with Christianen et al. (2017), the blue
mussel Mytilus edulis from deep channel buoys was
taken as a proxy for the pelagic baseline. In contrast to
Christianen et al. (2017), the common periwinkle Lit-
torina littorea was used, as it was considered to be the
best suitable proxy for the benthic baseline in the
Marsdiep area. These relatively large and long-lived
primary consumers integrate temporal variability,
thereby representing average δ15N baseline values.
M. edulis, an obligatory suspension feeder, was col-
lected just below the water surface from buoys in deep
channels. L. littorea was collected at various lo ca tions
in the intertidal. Isotopic values of M. edulis and L.
litto rea that were used had been collected be tween
2011 and 2014 from several locations (87 and 60,
respectively) in the western part of the Wadden Sea.
L. littorea feeds primarily on ephemeral filamen-
tous bladed algae, other macrophytic sporelings/
germlings and scraping surficial diatoms (Tyrrell et
al. 2008). To validate this species as a proxy for the
benthic baseline, δ13C values were compared with
those of benthic diatoms and Ulva lactuca and U.
N N N(TP– )
15 c15 b
δ=δ+Δλ
[C (C C)]/(TP )/ C C
13 b2 13 c13 b2 13 b1
()
α=δ−δ+Δ−λδ+δ
C C 2.21 0.82 C:N
13 corr 13 bulk
δ=δ−
118
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Poiesz et al.: Wadden Sea fish community explained through stable isotopes
ulva. The diatoms and Ulva samples had a temporal
(2011−2013) and spatial (western Wadden Sea) cov-
erage similar to the L. littorea data (see Christianen
et al. 2017). The δ13C values of L. littorea had a range
of −17.1 to −10.6‰ (average ± SE: −14.22 ± 0.18‰),
the Ulva species had a range of −18.47 to −9.15
(−13.91 ± 0.29‰) and the diatoms had a range of
−19.8 to −10.42‰ (−14.12 ± 0.17‰), justifying the use
of L. littorea as a proxy for benthic production.
The average (±SD) trophic fractionation factors of
3.4 ± 0.98‰ for δ15N and 0.39 ± 1.3‰ for δ13C were
taken from Post (2002). The 2 different baselines
were incorporated into the calculation together with
the variable trophic fractionation, using the TROPHIC-
POSITION R package (R Core Team 2019) with a
Bayesian TP model following Quezada-Romegialli et
al. (2018). Trophic fractionation for N in the Marsdiep
basin was estimated for the various functional groups
by determining the relationship between the esti-
mated average TP (TP
diet) of a fish species based on
stomach contents (taken from Poiesz et al. 2020) and
the mean δ15N value.
2.4. Trophic niche
Based on the δ15N and δ13C isotope values, trophic
niches were quantified for fish species using niche/
community metrics following Layman et al. (2007): (1)
δ13C range (CR), which represents the niche diversifi-
cation with respect to the basal food sources, whereby
higher CR reflected the utilization of a broader spec-
trum of food sources; (2) δ15N range (NR), which rep-
resents the vertical food web structure and therefore
the diversity of TPs, providing information on the
trophic length of the community; (3) total area (TA),
which is the convex hull area encompassed by all spe-
cies in the δ13C− δ15N bi-plot space, reflecting the size
of the total niche space occupied and (4) mean dis-
tance to centroid (CD), which is the mean distance of
the isotopic value of each specimen
from the δ15N−δ13C centroid and is a
proxy for trophic diversity. For the dif-
ferent species, the estimated isotopic
niche width, measured as the convex
hull TA and the standard ellipse areas
(SEA; ‰) and SEA corrected for small
sample sizes (SEAc; ‰) were calculated
using the corresponding trophic values
(δ15N and δ13C). Differences between
guilds and functional groups were de-
termined based on differences in TA
and SEAc.
Trophic redundancy (whereby species fill the
same trophic niche) was characterized by (1) the
mean nearest neighbour distance (MNND), which is
the mean distance in the isotopic space of each
predator to its nearest neighbour, and as such
reflects the average trophic (dis)similarity of preda-
tors and (2) the standard deviation of nearest neigh-
bour distance (SDNND), which is calculated as the
standard deviation of these distances and is a meas-
ure of the evenness of the spatial density and pack-
ing of the predators in the isotopic space. All
metrics were calculated using the Stable Isotope
Bayesian Ellipses in R (SIBER; Jackson et al. 2011)
package in the R statistical computing programme
(R Core Team 2019).
3. RESULTS
3.1. Stable isotopes
The pelagic δ13C baseline was −17.8 ± 0.1‰ and
the benthic baseline was −14.2 ± 0.1‰ (Table 1).
Freshwater and estuarine suspended organic matter
values were respectively in the range of −22 to −25
and −18 to −16‰. The δ13C values of the key prey
items of the fish fauna in the western Wadden Sea
varied from −15.9‰ for Gammarus sp. to −19.9
for Gastrosaccus spinifer (see Table S1 in the Sup -
plement at www. int-res. com/ articles/ suppl/ m677 p115
_ supp. pdf).
In total, 1658 samples from 57 fish species were
analysed (Table S2). The average δ13C values of the
Wadden Sea fishes varied from −11.3 to −27.0‰,
with most species within the range of −15 to −19
(Fig. 2). The golden grey mullet Chelon aurata had
the highest average δ13C value of −11.3‰, suggest-
ing macroalgae and/ or seagrass as a C source. Three
species had δ13C average values lower than −20‰:
round goby Neogobius melanostomus, vendace
119
Source Range Mean ± SE Source
(‰) (‰)
Pelagic
Freshwater SPOM −22 to −25 Jung et al. (2019)
Estuarine SPOM −18 to −16 Jung et al. (2019)
Mytilus edulis baseline −17.8 ± 0.1 Christianen et al. (2017)
Benthic
Littorina littorea −14.2 ± 0.1 Christianen et al. (2017)
Table 1. Overview of the δ13C baselines for the western Dutch Wadden Sea.
SPOM: suspended particulate organic matter
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Mar Ecol Prog Ser 677: 115–128, 2021
Coregonus albula and the eel
Anguilla anguilla, suggesting a fresh-
water C source. Pelagic species
showed δ13C values concentrated
around the pelagic baseline value
(Fig. 3A). The benthic species cov-
ered the whole δ13C range but most
species were also clustered around
the pelagic baseline value (Fig. 3A).
No differences were found between
the 3 guilds (Fig. 3C).
Average δ15N values varied from
13−18.3‰ among species (Fig. 2). The
thick-lipped grey mullet Chelon
labrosus, golden grey mullet, greater
120
Fig. 2. Average δ15N and δ13C stable iso-
tope values with standard error bars for
δ15N (vertical) and δ13C (horizontal) for all
Wadden Sea fish species. (A) Functional
groups; (B) guilds. The benthic baseline
and pelagic baseline are added for com-
parison. MSV: marine seasonal visitors;
JMM: juvenile marine migrants. For val-
ues and species names, see Table S2
Fig. 3. Frequency distri-
bution of average δ13C
(A,C) and δ15N (B,D) val-
ues for the Wadden Sea
fish species, by func-
tional groups (A,B) and
guilds (C,D). MSV: mar-
ine sea sonal visitors;
JMM: juvenile marine
migrants. Turquoise lines:
the pe lagic baseline of
Myti lus edulis (mean ±
SE δ13C: −17.8 ± 0.1 ‰);
dark green: benthic base -
line of Littorina littorea
(δ13C: −14.2 ± 0.1‰)
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Poiesz et al.: Wadden Sea fish community explained through stable isotopes
pipe fish Syn gnathus acus and 2 clupeoid species
pilchard Sardine pil char dus and anchovy Engraulis
encrasicolus had the lowest values around 13‰;
highest values around 17‰ were found for the twaite
shad Alosa fallax, smelt Osmerus eperlanus, cod
Gadus morhua, bass Dicentrarchus labrax, bull-rout
Myoxocephalus scorpius, tompot blenny Para-
blennius gattorugine, round goby and vendace. No
clear patterns were found in relation to functional
group (Fig. 3B) or guild (Fig. 3D).
Values of δ15N were significantly (p < 0.001) related
to fish size for some species; positively for bass, bib
Trisopterus luscus, bull-rout, cod, plaice Pleuro -
nectes platessa, sand-smelt Atherina presbyter and
sea trout Salmo trutta and negatively for herring Clu-
pea harengus (Table S3, Figs. S1 & S2). For all data of
all fish species together, the relationship was not sta-
tistically significant (F1,1447 = 0.54, p = 0.46). No sig-
nificant differences between years and season were
found for δ15N (t1470 = 0.316, p = 0.752; Fig. S3). In
addition, no significant relationship was found for
average fish length (cm) versus average δ15N (F1, 49 =
4.02, p = 0.051) and average δ13C (F1, 49 = 0.76, p =
0.387) (Fig. S4).
3.2. Trophic position
Mean TPs based on stable isotopes were estimated
for all fish species and ranged from 2.1−5.5, with the
majority between 2.2 and 3.5 (Fig. S5).
In line with δ15N, the 2 mullet species (thick-lipped
grey mullet, golden grey mullet), greater pipefish,
pilchard and anchovy had the lowest TPs. The less
common species (<10 observations) showed overall
the highest average TPs (vendace, forkbeard Phycis
blennoides, recticulated dragonet Callionymus reti -
culatus, houting Coregonus oxyrinchus, tompot blenny
and shanny Lipophrys pholis). Among the common
species (>10 observations), the highest TP va lues
were found for twaite shad, smelt, bull-rout and cod
(Fig. S5).
With respect to the different functional groups, the
few benthopelagic species had the smallest range,
and the benthic and pelagic group included the con-
sumers with the lowest TP values (mullet and clupeid
species). The highest TPs were almost the same in all
3 functional groups (Fig. S5). MSVs had the widest
range of TPs. JMMs, a small but abundant group of
juvenile flatfishes and clupeids, had the smallest
range (Fig. S5).
Mean TPs calculated based on stable isotope val-
ues were significantly lower than based on stomach
content data (F1,26 = 10.1, p < 0.05; Table 2). Only the
benthic species showed a significant relationship
between the calculated dietary-based TP and the
δ15N values (p > 0.05) (Fig. S6). For all species com-
bined, a trophic fractionation factor of 3.2‰ per
trophic level was found; for the groups separately:
benthic species 3.7‰, benthopelagic species 3.0
and pelagic species 1.0‰. The pelagic garfish Be -
lone belone and pilchard were outliers, as their stom-
ach content data indicated a mean TP value nearly
0.4 units higher than the δ15N TP estimates (Fig. S6;
lowest 2 blue dots).
3.3. Trophic niche
Density plots of SEA indicated a larger SEAc
for flounder Platichthys flesus, sea trout and thick-
lipped grey mullet compared to all other species
(Fig. 4, Table 3), which was due to large variability in
δ15N (sea trout) and δ13C (flounder), respectively, or
both (thick-lipped grey mullet).
With respect to functional groups, trophic niche
space was smallest for benthopelagic species and
overlapped with niches of both pelagic and benthic
species. The trophic niche space of benthic species
also overlapped with that of the pelagic species. In
benthic species, the largest range of δ13C values
were found compared to the benthopelagic and
pelagic species (Fig. 5).
In terms of guilds, trophic niche space was smallest
for JMM species (0.91). The trophic niche of both NR
species and MSVs overlapped with the niche of
JMM. The size of the trophic niche of both NR spe-
cies and MSVs was about the same but overlapped
partly with the highest TP values in NR species.
Highest δ13C values (−6.5 ‰) were found among the
MSV, and highest δ15N values (25‰) occurred in the
NR species (Figs. S1 & S2).
Trophic niche sizes were compared based on
their SEAc (Table 3). The Layman metrics for
trophic di versity and redundancy confirmed differ-
ences in the trophic structure of the different
groups and guilds (Table 4). The benthopelagic
group and JMMs had the smallest mean δ13C range
(CR = 2.02 and 2.55), while the MSVs and benthic
species had the highest (CR = 7.90 and 6.94). The
JMMs had the smallest range in δ15N (NR = 0.92)
and the benthic group had the highest (NR = 4.10).
The CD was smallest for the benthopelagic group
(0.82) (trophic diversity), where by the other groups
were found to be around 1. The smallest MNND
(0.60; trophic redundancy) was found for the NR
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Mar Ecol Prog Ser 677: 115–128, 2021
species and the highest (1.20) was found for the
MSV species. The highest convex hull areas (TA =
15.16 and 15.95) were observed for the benthic and
MSV species, while the smallest was found for
JMMs (Fig. 5).
4. DISCUSSION
Three different estimates of the
trophic structure of Wadden Sea
fish fauna are currently available:
estimates based on (1) FishBase
(Froese & Pauly 2019); (2) ‘snapshot’
dietary information from stomach
content data (Poiesz et al. 2020) and
(3) stable isotope fractionation (this
study). Focussing on the 28 most
abundant Wadden Sea fish species
(species with 10 or more obser -
vations), estimates of TP based on
stomach contents and FishBase were
generally similar, but also showed differences in
both directions. The estimate of TP based on
stable isotope data was on average about 20%
(varying from 4−33%) lower than the 2 other
estimates.
122
Common name Scientific name Functional Guild TP TP TP
group stomach Fish- isotope
content Base based
Bass Dicentrarchus labrax Benthic NR 3.70 3.50 3.42
Bib Trisopterus luscus Benthopelagic MSV 3.56 3.70 2.88
Bull-rout Myoxocephalus scorpius Benthic NR 3.57 3.90 3.52
Cod Gadus morhua Benthopelagic MSV 3.75 4.10 3.36
Dab Limanda limanda Benthic MSV 3.32 3.40 2.59
Five-bearded rockling Ciliata mustela Benthic NR 3.65 3.50 3.13
Flounder Platichthys flesus Benthic NR 3.47 3.30 3.12
Garfish Belone belone Pelagic NR 4.65 4.20 2.88
Golden grey mullet Chelon auratus Benthic MSV 2.13 2.80 2.32
Greater pipefish Syngnathus acus Benthic NR 3.60 3.30 2.37
Herring Clupea harengus Pelagic JMM 3.44 3.40 2.57
Pilchard Sardina pilchardus Pelagic MSV 3.52 3.10 2.24
Plaice Pleuronectes platessa Benthic JMM 3.23 3.20 2.73
Pollack Pollachius pollachius Benthopelagic MSV 3.70 4.30 3.25
Saithe Pollachius virens Pelagic MSV 4.13 4.30 2.84
Sand goby Pomatoschistus minutus Benthic NR 3.84 3.20 3.24
Sand-smelt Atherina presbyter Pelagic NR 3.26 3.70 3.06
Scad Trachurus trachurus Pelagic MSV 4.13 3.70 2.80
Sea trout Salmo trutta Peagic NR 4.58 3.40 3.05
Smelt Osmerus eperlanus Pelagic MSV 3.93 3.50 3.36
Sole Solea solea Benthic JMM 3.10 3.20 2.85
Sprat Sprattus sprattus Pelagic JMM 3.13 3.00 2.73
Stickleback Gasterosteus aculeatus Benthopelagic NR 3.13 3.30 3.00
Thick-lipped grey mullet Chelon labrosus Benthic MSV 2.36 2.60 2.33
Turbot Scophthalmus maximus Benthic MSV 3.85 4.40 3.14
Twaite shad Alosa fallax Pelagic NR 3.86 4.00 3.20
Viviparous blenny Zoarces viviparus Benthic NR 3.46 3.50 3.13
Whiting Merlangius merlangus Benthopelagic MSV 3.64 4.40 3.13
Table 2. Functional group, guild and mean trophic position (TP) for Wadden Sea fish species with more than 10 observations
based on stomach content analysis after Poiesz et al. (2020), FishBase (www.fishbase.org) and stable isotope analysis (this study)
Fig. 4. Density plots of corrected standard ellipse areas (SEAc) (black dots) for
all Wadden Sea species with more than 10 observations with credible intervals
(50% inside dark grey boxes, 75% middle grey boxes, 95% outer light
grey boxes)
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Poiesz et al.: Wadden Sea fish community explained through stable isotopes
4.1. What is fuelling the Wadden Sea
fish food web?
ENA for various periods in different parts of the
Wadden Sea (Balgzand NL; Jade Germany; Sylt-
Rømø Germany/DK) illustrated large spatial and
temporal variability in the contribution of various
local producers versus imported organic matter as
the energy source of the local food web (Baird et al.
2012, Schückel et al. 2015, Jung et al. 2020). Despite
a small enrichment relative to the diet, carbon iso-
topic values can be used to identify the main energy
sources of a species as they reflect their diet within
about 1‰ (for overview see Michener & Kaufman
2007). For the Dutch part of the Wadden Sea, Chris-
tianen et al. (2017) concluded, from an extensive
stable carbon isotope analysis, that local benthic pri-
mary producers were the most important energy
source for the majority of the intertidal macrozoo -
benthic food web. Due to the almost complete
absence of macroalgae in this area (Folmer et al.
2016), microphytobenthos appears to be the most
123
Fig. 5. Total convex hulls area for the (A) various functional
groups and (B) guilds based on mean isotope values of the
individual Wadden Sea fish species with more than 10
observations. MSV: marine seasonal visitors; JMM: juvenile
marine migrants. (C,D) Density plots of standard ellipses
areas (black dots) for the (C) 3 functional groups and (D)
guilds with credible intervals (50% inside dark grey boxes,
75% middle grey boxes, 95% outer light grey boxes)
Common name TA SEA SEAc
Bass 87.61 7.53 7.56
Bib 5.51 1.99 2.11
Bull rout 2.14 0.80 0.86
Cod 6.66 2.77 2.89
Dab 8.56 1.19 1.20
Five bearded ockling 11.86 2.23 2.27
Flounder 119.18 13.47 13.54
Garfish 14.43 3.70 3.85
Golden grey mullet 48.21 7.78 7.90
Greater pipefish 5.68 1.85 1.95
Herring 42.62 6.57 6.61
Pilchard 10.65 3.60 3.78
Plaice 28.53 5.62 5.68
Pollack 9.14 3.89 4.17
Saithe 5.93 3.83 4.37
Sand goby 6.38 2.35 2.52
Sand smelt 5.20 1.89 1.97
Scad 18.10 4.49 4.60
Sea trout 78.82 13.05 13.22
Smelt 23.77 3.92 4.04
Sole 3.65 1.70 1.91
Sprat 11.25 3.29 3.42
Stickleback 6.33 2.04 2.12
Thick lipped grey mullet 106.43 14.80 15.07
Turbot 4.14 1.50 1.59
Twaite shad 32.53 5.27 5.35
Viviparous blenny 3.18 1.27 1.37
Whiting 23.03 3.52 3.58
Table 3. Convex hull area (TA) and standard ellipse areas
(SEA, ‰) for Wadden Sea fish species with more than 10 ob -
servations. SEAc: SEA corrected for a small sample size,
representing the isotopic niche metrics calculated for all
species in sympatry based on the δ15N and δ13C values
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Mar Ecol Prog Ser 677: 115–128, 2021
important energy source for the majority of the inter-
tidal benthic food web (Christianen et al. 2017).
Recently, Jung et al. (2020) confirmed the dominant
role of microphytobenthos as primary producers in
the Balgzand intertidal area in the western Wadden
Sea.
In our study, most Wadden Sea fish species had
δ13C values in the range of −15 to −20‰, whereby
pelagic species could be distinguished by their lower
stable carbon signals compared to benthic and ben-
thopelagic species, in line with the proxy for pelagic
primary producers (Currin et al. 1995, Stribling &
Cornwell 1997, Riera et al. 1999). The diet of the
western Wadden Sea fish fauna shows a large prey
overlap, with a focus on a few key species: amphipod
crustaceans, brown shrimps, juvenile herring and
gobies (Poiesz et al. 2020). For most of the benthic
and benthopelagic species, macrozoobenthic prey is
(part of) their diet (Poiesz et al. 2020), and therefore
microphytobenthos will also be an important energy
source (Christianen et al. 2017) for these functional
groups. In addition, most benthic and benthopelagic
species also prey partly upon the epibenthic key
items, with a more pelagic signal such as, for in -
stance, copepods consuming juvenile herring. There -
fore, in the shallow Wadden Sea, microphytoplank-
ton will not only be an important energy source for
the pelagic fish fauna but also for some benthic and
epibenthic fish species, as reflected in their relatively
low δ13C isotope values. The absence of a clear pat-
tern between the various guilds, NR species, JMMs
and MSVs indicates that their main energy source
constitutes prey items from ‘local production’.
Some fish species had very high or very low δ13C
values. Golden grey mullet had the highest δ13C
value of around −11.3‰, which points to seagrasses
and/or marine macroalgae as their main energy
source. On the other hand, eels had a very low δ13C
value of about −27‰. These eels were
large migrating females caught in
autumn, so their δ13C values probably
indicate a freshwater origin (Harrod et
al. 2005, Middelburg & Herman 2007).
Our results for the western Wadden
Sea are consistent with data of the fish
fauna in the Sylt-Rømø basin in the
eastern part of the Wadden Sea (de la
Vega et al. 2016). In the Sylt-Rømø
basin, δ13C values ranged on average
from −16 to −19‰, and differences in
pelagic, benthopelagic and benthic
species were also found. Some other
studies point to large differences be -
tween habitats. For in stance, in the Gi ronde estuary
along the French west coast, most fish species had
different stable carbon isotope values in different
habitats along a salinity gradient (Selles lagh et al.
2015). Also, in saltmarsh areas, fish species will
assimilate material derived from macrophytes and
filamentous algae (see for instance Winemiller et al.
2007). In general, local morphological and hydro-
graphical characteristics will (indirectly) affect the
δ13C values of the fish fauna.
4.2. Wadden Sea fish food web
The calculation of TPs for the various Wadden Sea
fish species in this study is based on a mean fraction-
ation of 3.4‰ for δ15N, which was derived for a wide
range of consumers by van der Zanden & Rasmussen
(2001) and Post (2002). However, this calculation of
TP can only be considered as a rough estimate given
the large variability in fractionation on the order of
1.8‰ (van der Zanden & Rasmussen 2001).
The majority of calculated TPs based on stable iso-
topes of the western Wadden Sea fish species ranged
from 2.2−3.5, with most TPs above 2.5. Except for the
low TPs of mullets and clupeids (herring, sprat
Sprattus sprattus and pilchard) that consume algae
(Poiesz et al. 2020), the range in TPs was similar for
the different functional groups (pelagic, bentho -
pelagic, benthic). With respect to guild, MSVs had
the largest range of TPs and JMMs, the smallest.
Maximum TPs of the JMM using the area as a nurs-
ery (Zijlstra 1983) were between 3.0 and 3.5, which is
a medium TP.
The TPs estimated from stomach content data re-
sulted in higher values, ranging from 2.0−4.7, and
with most TPs above 3.0 (Poiesz et al. 2020). A possi-
ble reason for this mismatch between TP based on
124
Benthic Bentho- Pelagic (Near-) JMM MSV
pelagic resident
NR 4.104 1.513 3.728 3.59 0.915 3.854
CR 6.949 2.026 3.075 3.669 2.557 7.908
TA 15.164 1.518 6.063 6.414 1.199 15.951
CD 1.748 0.822 1.223 1.236 1.046 1.852
MNND 1.000 0.725 0.805 0.608 0.879 1.208
SDNND 1.286 0.646 0.409 0.459 0.237 1.349
Table 4. Layman metrics for the functional groups and guilds of Wadden Sea
fish species (JMM: juvenile marine migrant; MSV: marine seasonal visitor).
CR: δ13C range; NR: δ15N range; TA: convex hull area; CD: mean distance
to centroid; MNND: mean nearest neighbour distance; SDNND: standard
deviation of nearest neighbour distance
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Poiesz et al.: Wadden Sea fish community explained through stable isotopes
stable isotopes and dietary-based TP might be that
sedimentary organic matter, microbial biomass and
smaller benthic marine microphytobenthos were not
identified in the stomach contents of (benthic) pre -
dators. The exclusion of these ‘lower’ trophic food
sources would therefore result in an overall overesti-
mation of the TP from diet. The low isotope-based
TPs found for both some benthopelagic and pelagic
species might be explained by their diet, such as the
benthopelagic bib feeding on a wide variety of differ-
ent smaller prey items like mysidacea and small crus-
taceans (among others; Heessen et al. 2015, Poiesz et
al. 2020) and the pelagic herring, pilchard and sprat,
which feed mainly on copepods, bristle worms, mysi-
dacea and small shrimps (Poiesz et al. 2020). An alter-
native explanation might be that our baseline species
are not 100% herbivorous in the area.
Part of the discrepancy is because the trophic frac-
tionation differs from the average value of 3.4 ‰ from
van der Zanden & Rasmussen (2001) and Post (2002)
and that this trophic fractionation is species-specific.
According to Minagawa & Wada (1984), van der Zan-
den & Rasmussen (2001) and Goedkoop et al. (2006),
trophic fractionation values could range between 1
and 9‰, depending on diet and environmental fac-
tors. This study showed indeed that trophic fraction-
ation differed at the functional group level, with a
slightly higher value of 3.7‰ for benthic species and
a somewhat lower value (3.0‰) for benthopelagic
species. For the pelagic species, a relatively low
value on the order of 1.0‰ was found. Diet quality
and food processing mechanisms may affect fraction-
ation (Mill et al. 2007). Therefore, calculating the dif-
ferent trophic fractionation values is a useful tool for
distinguishing different fish species. Estimates of TP
are more sensitive to assumptions and different life-
history traits about the trophic fractionation of δ15N
than to the isotopic baseline (Post 2002).
The trophic structure of the western Wadden Sea
fish community still includes predatory fishes with a
TP above 3.0, and maximum TPs are comparable to
the TPs observed in other coastal European areas
such as the Tagus estuary (Vinagre et al. 2012),
where larger more pelagic species showed higher
values than smaller benthic species. However, these
values are lower than documented for coastal zones
(see for instance Rodríguez-Graña et al. 2008). The
ab sence of the highest TPs might be due to the loss
of predatory species in the Wadden Sea. Whereas
skates and sharks used to be common in the North
Sea and surrounding coastal areas, they are now
either absent or occur in low densities (Wol 2005).
Predatory shark and skate species had TPs (based on
historical archive dietary data) in the range of 3.2−4.6
(Poiesz et al. 2021). Another explanation might be
due to trophic downgrading, where food webs lose
complexity and trophic biodiversity due to changing
environmental conditions (changing temperatures,
eutrophication) and competition (Saleem 2015,
Edwards & Konar 2020, Yan et al. 2020).
4.3. Trophic niche
For the Wadden Sea fish species, stable isotope
values (both δ13C and δ15N) did not vary significantly
between spring and autumn. Some species showed a
significant (p < 0.001) increase (for δ13C: herring and
sea trout; for δ15N: bass, bib, cod, plaice, sea trout,
twaite shad) and some others showed a significant
decrease with size (for δ13C: bass, whiting Merlan -
gius merlangus, sole Solea solea; for δ15N: herring,
thick-lipped grey mullet). For bass, these findings
are in line with the significant relationship found by
Cardoso et al. (2015).
Spring catches contain fish migrating from the
North Sea into the Wadden Sea whilst autumn catch -
es include the locally produced young-of-the-year
(Fonds 1983). The absence of a difference in stable
isotope values between spring and autumn suggests
that the trophic niche of the various fish species in
the coastal zone and inside the Wadden Sea is simi-
lar. Stomach content composition also did not differ
with fish size or between spring and autumn (Poiesz
et al. 2020).
The average stable isotope values for Wadden Sea
fish species cover a large range for δ13C, from −13
to −27‰ and for δ15N, from 13.5 to 18.5 and
clearly differ among species, illustrating high trophic
diversity in the area whereby various species occupy
different niches. Trophic niche size (SEA, SEAc) was
more or less similar for most of the Wadden Sea fish
species, except for a few with large variability. These
species (flounder, thick-lipped grey mullet and gol -
den grey mullet [diadromous] and sea trout [anadro-
mous]) are species which are tolerant to both seawa-
ter and freshwater during their life cycle and hence
have a large trophic niche size. Both the functional
groups (benthic, benthopelagic, pelagic) and guilds
(NR, JMM and MSV) showed trophic niche overlap
to a large extent, illustrating trophic competition
(Dubois & Colombo 2014).
Trophic competition appears to be most visible for
JMMs (nursery-type species), mainly consisting of
pelagic juvenile clupeid species and benthic juvenile
flatfish species (van der Veer et al. 2015). This re -
125
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Mar Ecol Prog Ser 677: 115–128, 2021
flects the prey overlap in the diet, as also found in the
stomach content analysis, whereby a few key prey
species (amphipods, brown shrimps, juvenile herring
and gobies) could be identified (Poiesz et al. 2020).
Present information indicates that for juvenile flat-
fish, resource limitation does not seem to be an issue:
growth during most of the summer is maximum and
determined by water temperature only (van der Veer
et al. 2016). The same holds true for the abundant
group of gobies (Freitas et al. 2011). Present growth
conditions and competition among juvenile clupeid
species in the Wadden Sea are unclear.
Data archive. Original data and R script for calculations can
be found at https://dx.doi.org/10.25850/ nioz/7b.b.bb.
Acknowledgements. Thanks to all of our colleagues, espe-
cially Rob Dapper, Ewout Adriaans, Willem Jongejan, Sieme
Gieles and Marco Kortenhoeven, for assisting in the collec-
tion of the samples, and to Thomas Leerink, David Zaat and
Vincent van Ernich for grinding, homogenizing and weight-
ing of the stable isotope samples. All fish sampling and
handling was done under CCD project number AVD
8020020174165. Key prey species were collected within the
framework of ZKO project 839.08.242 of the National Ocean
and Coastal Research Programme (ZKO), supported by The
Netherlands Organization for Scientific Research (NWO).
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