Changes in functioning of the largest coastal North Sea flatfish nursery, the Wadden Sea, over the past half century

Abstract

The international Wadden Sea is an important flatfish nursery. Information from the Dutch Wadden Sea indicates that the flatfish nursery function of the area has been affected during the last decades. Increased seawater temperature has affected settling, habitat suitability for and growth performance of the various flatfish species. Settling of plaice, flounder and to a lesser extent sole larvae occurs earlier nowadays. In the 1960s, 0-, I-, II- and III-group plaice were present, but since 2000, II-group has disappeared and densities of I-group have decreased. For juvenile flounder, II-group almost disappeared, and for dab, a decline in densities of all age groups was observed from the 1990s onwards. Summer temperatures exceed the optimum for the cold-water species (plaice, flounder and dab) with increasing frequency, level and duration. Only for 0-group sole, the period with optimal growth conditions has become longer and has resulted in increased growth. Mortality rates in 0-group plaice have increased, coinciding with an increase in water temperatures and an increase in the abundance of predators. The decrease in density of juvenile plaice and dab in the Wadden Sea has not affected recruitment to North Sea stocks, suggesting that other areas have taken over part of the nursery function. The predicted increase in seawater temperature in the next decades will continue to improve the conditions for sole. The temperature tolerance of plaice and dab and to a lesser extent flounder will further reduce their scope for growth and may ultimately result in their disappearance from the Wadden Sea.

Full text

MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 693: 183–201, 2022
https://doi.org/10.3354/meps14082 Published July 21
1. INTRODUCTION
The temperate North Sea harbours an important
and abundant group of flatfish species, each of which
is characterised by a specific life cycle, habitat
requirements and distribution (Heessen et al. 2015).
The juvenile stages of a number of these species,
such as plaice Pleuronectes platessa, flounder
Platichthys flesus, sole Solea solea, brill Scophthal-
mus rhombus, turbot Scophthalmus maximus and to
© The authors 2022. Open Access under Creative Commons by
Attribution Licence. Use, distribution and reproduction are un -
restricted. Authors and original publication must be credited.
Publisher: Inter-Research · www.int-res.com
*Corresponding author: henk.van.der.veer@kpnmail.nl
REVIEW
Changes in functioning of the largest coastal
North Sea flatfish nursery, the Wadden Sea,
over the past half century
Henk W. van der Veer1,*, Ingrid Tulp2, Johannes IJ. Witte1, Suzanne S. H. Poiesz1,3, 5,
Loes J. Bolle2,4
1NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, PO Box 59, 1790 AB Den Burg Texel,
The Netherlands
2Wageningen University & Research, Wageningen Marine Research, PO Box 68, 1970 AB IJmuiden, The Netherlands
3Faculty of Science and Engineering, Groningen Institute of Evolutionary Life Sciences, University of Groningen,
PO Box 11103, 9700 CC Groningen, The Netherlands
4Nouvelle-Aquitaine Eco Studies, 23400 Saint-Moreil, France
5Present address: Wageningen University & Research, Wageningen Marine Research, PO Box 77, 4400 AB Yerseke,
The Netherlands
ABSTRACT: The international Wadden Sea is an important flatfish nursery. Information from the
Dutch Wadden Sea indicates that the flatfish nursery function of the area has been affected during
the last decades. Increased seawater temperature has affected settling, habitat suitability for and
growth performance of the various flatfish species. Settling of plaice, flounder and to a lesser
extent sole larvae occurs earlier nowadays. In the 1960s, 0-, I-, II- and III-group plaice were pres-
ent, but since 2000, II-group has disappeared and densities of I-group have decreased. For juve-
nile flounder, II-group almost disappeared, and for dab, a decline in densities of all age groups
was observed from the 1990s onwards. Summer temperatures exceed the optimum for the cold-
water species (plaice, flounder and dab) with increasing frequency, level and duration. Only for 0-
group sole, the period with optimal growth conditions has become longer and has resulted in
increased growth. Mortality rates in 0-group plaice have increased, coinciding with an increase in
water temperatures and an increase in the abundance of predators. The decrease in density of
juvenile plaice and dab in the Wadden Sea has not affected recruitment to North Sea stocks, sug-
gesting that other areas have taken over part of the nursery function. The predicted increase in
seawater temperature in the next decades will continue to improve the conditions for sole. The
temperature tolerance of plaice and dab and to a lesser extent flounder will further reduce their
scope for growth and may ultimately result in their disappearance from the Wadden Sea.
KEY WORDS: Wadden Sea · Nursery function · Juvenile flatfish · Long-term trends · Climate
change · Species composition · Growth · Mortality
O
PEN
PEN
A
CCESS
CCESS

Mar Ecol Prog Ser 693: 183–201, 2022
a lesser extent dab Limanda limanda, concentrate in
relatively shallow coastal nursery areas around the
North Sea. The international Wadden Sea and its
coastal zone (water depth <10 m), bordering the
western coast of Denmark and the northern coasts of
Germany and The Netherlands, has historically been
the largest juvenile flatfish nursery in the North Sea
(Zijlstra 1972, van Beek et al. 1989).
The use of coastal areas as nursery grounds was
already observed during the first investigations in
Danish (Petersen 1895, Johansen 1913) and Dutch
waters (Redeke 1905). The first quantitative inven-
tory in the western Dutch Wadden Sea in 1961−1964
(Creutzberg & Fonds 1971) found numerous juvenile
plaice, flounder, sole and dab in the subtidal and
deeper parts (Fonds 1983). Both the annual Demersal
Fish Survey (DFS) carried out from the early 1970s
onwards (Zijlstra 1972) and the bycatch data of the
shrimp Crangon crangon fishery confirmed these
observations. An analysis of the first decades of the
annual DFS concluded that the Wadden Sea was an
important nursery area for plaice and sole contribut-
ing substantially to annual recruitment and that
abundance indices of 0-group plaice and I-group
sole were correlated with recruitment rates to the
North Sea fishery stocks (Rauck & Zijlstra 1978, van
Beek et al. 1989).
Worldwide, coastal ecosystems are critical transi-
tion zones between freshwater and marine environ-
ments (Beck et al. 2001, Levin et al. 2001). For cen-
turies, such areas have suffered from anthropogenic
disturbance including fisheries, port activities, eu -
trophication and land reclamation. Such activities
have caused major structural and functional changes
(Jackson et al. 2001, Lotze 2005, Lotze et al. 2006).
The Wadden Sea has also experienced major ecosys-
tem changes (for an overview, see Kloepper et al.
2017).
In the western Dutch Wadden Sea, sea surface
temperature (SST) measurements from 1947 on -
wards show that annual means varied around 10°C
until 1982, but thereafter increased to about 12°C in
recent years. This increase occurred for all seasons at
an average rate of about 1°C per 20−25 yr (van Aken
2008a, Royal Netherlands Institute for Sea Research
[NIOZ] unpubl.). Increases in SST are not restricted
to the Wadden Sea and occur in the whole Dutch
coastal zone (van Aken 2010). In the 1980s, eutroph-
ication doubled the nutrient concentrations in the
western Dutch Wadden Sea (van der Veer et al. 1989,
van Raaphorst & de Jonge 2004), resulting in a period
of increased chlorophyll concentrations and primary
production (Philippart et al. 2007). Since the 1990s,
annual planktonic primary production has decreased
and recently stabilized (Jacobs et al. 2020). The
increased chlorophyll concentrations and planktonic
primary production resulted in a doubling of the
macrozoobenthic biomass in the intertidal areas
(Beukema & Dekker 2020). During the subsequent
period of de-eutrophication, reduced primary pro-
duction did not cause a decrease in macrozoobenthic
biomass (Beukema & Dekker 2020).
Predation pressure by top predators has also
increased strongly since the 1990s as a result of an
increased abundance of cormorants Phalacrocorax
carbo, harbour seals Phoca vitulina and grey seals
Halichoerus grypus (for references see van der Veer
et al. 2015a). Commercial shrimp fisheries, an impor-
tant source of bycatch-induced fish mortality in the
Wadden Sea, also increased strongly during the last
decades (van der Hammen et al. 2015, van der Veer
et al. 2015a). In the western part of the Wadden Sea,
catches of both pelagic and demersal fish showed a
10-fold decrease from the late 1970s before stabiliz-
ing in the late 1990s (Tulp et al. 2008, van der Veer et
al. 2015a). Densities of scavengers and benthic pred-
ators such as shore crabs increased strongly since the
early 2000s (Tulp et al. 2012), simultaneously with the
recovery of mussel beds (van der Meer et al. 2019).
The combined impact of these major changes in
the Wadden Sea ecosystem on the flatfish nursery
function is unclear. For the flatfish nursery function
of the Wadden Sea, 2 aspects are important: (1) the
local hydrodynamic and morphodynamic conditions
in the coastal zone and tidal inlets that provide con-
nectivity for the drifting pelagic larval stage in
the North Sea with the areas in the Wadden Sea used
by the subsequent juvenile life stage, and (2) the pro-
vision of essential demersal habitats for juveniles
which ultimately contribute to the recruitment to the
North Sea fish stocks. The connectivity between lar-
val habitat in the North Sea and demersal habitat for
juveniles in the coastal area has been described by
van der Veer et al. (1998), Bolle et al. (2009), Hufnagl
et al. (2013) and Tiessen et al. (2014).
This paper addresses the importance of the Wad-
den Sea in providing essential demersal habitat for
juveniles and its contribution to recruitment to the
North Sea fish stocks. The focus is on the boreal
(cold-water) species plaice, flounder and dab and on
the Lusitanian (warm-water) species sole (Fonds
1983). First, the species-specific physiological per-
formance of the various flatfish species is described.
Next, based on the changes in the Wadden Sea over
the last 50 yr, expectations on the impact on the flat-
fish nursery functioning of the area are formulated
184

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning
and reviewed. This paper focusses on the western
part of the Wadden Sea, is based on both published
and unpublished data and elaborates on previous
studies presenting aspects of the flatfish nursery
function of the Wadden Sea (van der Veer &
Bergman 1987a, Bergman et al. 1988, Lozán et al.
1994).
2. FLATFISH PHYSIOLOGICAL PERFORMANCE
Poikilothermic marine organisms are affected dif-
ferently by physical factors, depending on their spe-
cies-specific physiological preferences and tolerance
(for an overview, see Willmer et al. 2000). Within the
full range of physical factors, water temperature is
the controlling factor regulating and dictating meta -
bolism; salinity is a masking factor loading meta -
bolism and thereby creating sub-optimal conditions;
and oxygen conditions are a limiting factor constrain-
ing maximum possible metabolic scope (Fry 1971,
Neill et al. 1994).
The Wadden Sea is a dynamic area with abiotic
conditions varying spatially and temporally at a scale
ranging from, respectively, tidal gully to tidal basin
and tide to year (e.g. van Aken 2008a,b). In the Wad-
den Sea, water temperature is among the most
important factors controlling and regulating metabo-
lism and hence growth (e.g. see Fonds et al. 1992). At
present, profound salinity gradients occur only in the
few remaining open estuarine basins, the Ems Dol-
lard and the Elbe. Oxygen deficiencies including
sediment black spots occurred in the 1990s espe-
cially in the German part of the Wadden Sea (Neira &
Rackemann 1996, Böttcher et al. 1998), but during
the last decades, this phenomenon has not been
reported.
For many flatfish species and life stages, basic
information about the effect of various factors on
metabolism is scarce, and most available information
deals with the impact of temperature as a controlling
factor. Some experimental studies addressed the
effect of temperature in combination with salinity as
a masking factor (Fonds et al. 1992, Augley et al.
2008), or in combination with oxygen as a limiting fac-
tor (Pörtner & Knust 2007). The sensitivity for envi-
ronmental factors is often species- and size- specific
with a well-defined tolerance range. From the juve-
nile stage onwards, flatfish may also be able to avoid
unfavourable masking and limiting conditions in the
field by active migration.
Thermal tolerance ranges are determined by the
combined impact of the rate-enhancing influence
of temperature on enzyme function ultimately re -
flected in growth and the increasing destructive
effects, especially structural damage (Willmer et al.
2000). As a consequence, physiological performance
(such as growth) increases with temperature until a
maximum rate is reached (at the optimum tempera-
ture), followed by an abrupt decrease to zero.
Within the tolerance range, a temperature prefer-
ence range can be defined where growth rates
exceed a certain minimum (Fig. 1).
Temperature tolerance and optimum
are often determined under experimen-
tal laboratory conditions.
Experimental data indicate that the
temperature tolerance of plaice eggs and
larvae ranges from 2°C to at least an
optimal temperature of 10°C (Ryland et
al. 1975), similar to that for flounder
larvae (Hiddink 1997). For dab, no ex -
perimental data are available, but in
the North Sea, developing larvae were
found within a temperature range of 4 to
10°C (Malzahn et al. 2007). For sole eggs
and larvae, the temperature tolerance
ranges from 10°C to at least 19 and 22°C,
respectively (Fonds 1979). For all spe-
cies, the upper temperature tolerance
limits of the eggs and larvae are unclear.
For juvenile flatfish, more detailed infor-
mation is available (Fig. 2). 0-group sole
has the largest temperature tolerance
185
Fig. 1. Flatfish thermal tolerance range. Dashed line indicates selected min-
imum growth rate (here 10% of the maximum growth rate). Blue: lower
temperature range with growth rates <10% of the maximum growth rate at
the optimal temperature; green: range of temperatures with increasing
growth rates until maximum growth at the optimal temperature; orange:
range of temperatures above optimal temperature with decreasing growth
rates until 10% of the maximum growth rate; red: temperatures above
which growth becomes <10 % of the maximum growth. The green and
orange area define the preference range within the tolerance range

Mar Ecol Prog Ser 693: 183–201, 2022
range including the highest temperatures (4−35°C)
(Lefrançois & Claireaux 2003); 0-group dab has the
narrowest and lowest range (0−22°C) (Fonds & Rijns-
dorp 1988); 0-group plaice (0−25°C) and flounder
(2−25°C) are intermediate in extent and level of tem-
perature tolerance (Fonds et al. 1992). The optimum
temperature varies from 15°C in juvenile dab, 18°C
in juvenile flounder, 19°C in juvenile plaice to 26°C
in juvenile sole (Fig. 2). Overall, flatfish eggs and lar-
vae have narrower temperature tolerance ranges
than juveniles (see also Dahlke et al. 2020).
3. WADDEN SEA ECOSYSTEM CHANGES AND
EXPECTED IMPACT ON FLATFISH NURSERY
FUNCTIONING
Based on the observed changes in the Wadden Sea
ecosystem, expectations about potential impacts on
the flatfish nursery function of the area are formu-
lated. With respect to the effect of climate change,
we build on the study of climate effects on fish popu-
lations by Rijnsdorp et al. (2009).
3.1. Expectation 1: Coastal warming advances
larval flatfish immigration
Egg development rates are species-specific and
are determined by a variety of factors including in
particular seawater temperature. Egg development
rates are inversely related to seawater temperature
(e.g. Pauly & Pullin 1988). Larval stage duration is
also inversely related to seawater temperature (e.g.
Bolle et al. 2009). From hatching onwards, feeding
starts and larval stage duration also depends on food
abundance, whereby food limitation increases dev -
elopment time. Consequently, larval development
depends on the interplay between temperature and
food conditions. Field studies of drifting plaice larvae
in the Southern Bight of the North Sea observed an
inverse relationship between larval stage duration
and seawater temperature, albeit less strong than
expected based on experimental data (van der Veer
et al. 2009). Warming of the Dutch coastal zone is
expected to accelerate egg and larval development
and to advance the timing of flatfish immigration in
spring.
3.2. Expectation 2: Effect of increased seawater
temperature on spatial distribution and growth
potential is species-specific
Temperature preference and tolerance differ be -
tween flatfish species, with ranges varying from 20°C
for dab to 30°C for sole (Fig. 2). Temperature optima
also differ, from 15°C for juvenile dab, 18°C for juve-
nile flounder, 19°C for juvenile plaice to 26°C for
juvenile sole (Fig. 2). In the western Dutch Wadden
Sea, mean summer seawater temperatures in the
Marsdiep tidal inlet already exceeded the optimum
temperature for the 0-group dab in the late 1940s
(Fig. 3). For the 0-group flounder and plaice, mean
summer temperatures are still within their respective
tolerance ranges but have reached or even exceeded
their optimum temperature in the last decades. For 0-
group sole, mean summer seawater temperatures are
still below their optimum temperature. Shallower
waters, such as intertidal areas, will warm up even
more and will experience even larger fluctuations
and maximum water temperatures (van der Veer &
Bergman 1986, Frölicher & Laufkötter 2018). For
cold-water species, the water temperature in the
Wadden Sea increasingly exceeds their temperature
optimum and preference.
3.3. Expectation 3: Increased top predator
abundance and fisheries have increased flatfish
mortality
Juvenile flatfish are prey to a wide range of preda-
tors such as larger fish, seals and piscivorous birds.
Various fish species in the Wadden Sea (including
flatfish) consume juveniles, both in the intertidal and
186
08
16 24 32
0-group sole
0-group flounde
r
0-group dab
0-group plaice
Temperature (°C)
Fig. 2. Thermal tolerance range for 0-group
sole, flounder, dab and plaice. Temperature tol-
erance range (combined blue, green, orange
and red bar), optimal temperature (maximum of
green bar), and temperature preference range
(green + orange bar) for various flatfish species
and age groups. Temperature preference range
is defined as the temperature range with growth
rates >10 % of maximum rate at optimal temper-
ature (see Fig. 1 for more detail). For references,
see Section 2. Data from Freitas et al. (2010)

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning
in the subtidal (Fig. 4). Seals in the Wadden Sea feed
predominantly on juvenile flatfish, resulting in sub-
stantial mortality (Aarts et al. 2019). Cormorants are
important fish-eating birds in the Wadden Sea, and
flatfish comprise a large part of their diet. Based on
otoliths in regurgitated pellets, the average contribu-
tion of flatfish in the diet was estimated at 73% in
numbers and 79% in mass (Leopold et al. 1998).
Bycatch mortality from shrimp fisheries is also sub-
stantial (Glorius et al. 2015). The increase in popula-
tions of seals (since the 1990s) and fish-eating birds
(since the 1970s), as well as bycatch mortality (since
the 1970s) will have increased flatfish mortality in the
area.
187
8
9
10
11
12
13
Mean water temperature (°C)
-5
0
5
10
15
20
1940 1950 1960 1970 1980 1990 2000 2010 2020
1940 1950 1960 1970 1980 1990 2000 2010 2020
winter spring summer autumn
Mean water temperature (°C)
ab
Fig. 3. Water temperature in the Marsdiep inlet at the Royal
Netherlands Institute for Sea Research (NIOZ) jetty (1.5 m
below surface) for the period 1947−2020. (a) Mean annual
water temperature. (b) Mean winter (December−February),
spring (March−May), summer (June−August) and autumn
(September−November) water temperature. Data from
NIOZ (van Aken 2008a, S. van Leeuwen unpubl.)
0
10
0
10
0
10
0
10
0
10
0
10
10 20 30 40 50 60 70 80 90 100 110
Consumed plaice size (mm)
IS
A. cataphractus
(hooknose)
S. acus
(greater pipefish)
C. labrosus
(thicklipped grey mullet)
P. flesus
(flounder)
P. platessa
(plaice)
S. maximus
(turbot)
S. solea
(sole)
A. fallax
(twaite shad)
Z. viviparus
(eelpout)
C. lucerna
(tub gurnard)
D. labrax
(sea bass)
Number of prey (n)
Fig. 4. Size-frequency dis-
tribution of 0-group plaice
consumed in the intertidal
and the subtidal by various
fish species in the western
Dutch Wadden Sea. Data
based on stomach content
analysis of NIOZ fyke
catches 2011−2018 (Poiesz
et al. 2020, NIOZ unpubl).
Indicated is predator distri-
bution: I: intertidal; S: sub-
tidal. Grey: present; white:
absent

Mar Ecol Prog Ser 693: 183–201, 2022
3.4. Expectation 4: Year-class strength of cold-
water species will decrease in response to
increased seawater temperatures offshore
Year-class strength and ultimate recruitment in
fish are primarily determined by mortality processes
operating during the pre-juvenile stage of the life
history (Leggett & DeBlois 1994), and flatfish are no
exception (Brander & Houghton 1982, van der Veer
et al. 2015b). Interannual variability in year-class
strength is generated during the pelagic egg and
larval stage, probably by variations in the hydrody-
namic circulation (Bolle et al. 2009) and in mortality
rates of eggs and larvae (Harding et al. 1978, van der
Veer et al. 2000a). For most species, the underlying
mechanisms are unclear. Settling plaice larvae in the
western Wadden Sea originate mainly from the
spawning location in the Southern Bight of the North
Sea (Talbot 1977, Bolle et al. 2009), and year-class
strength is inversely related to seawater temperature
during egg and larval development (Brander &
Houghton 1982, van der Veer 1986, Fox et al. 2000).
Year-class strength of plaice may therefore decrease
in response to the increase in seawater temperature
in the coastal zone (van Aken 2010), and this may
also hold for other cold-water species.
4. CHANGES IN WADDEN SEA NURSERY
FUNCTIONING
4.1. Expectation 1: Coastal warming advances
larval flatfish immigration
Recent information about larval supply to the Wad-
den Sea is not available; however, the patterns in
abundance of settling and just-settled flatfishes pro-
vide an indication of both timing and abundance of
larval supply (van der Veer 1986). Such data are
available for the Balgzand intertidal area located in
the western Wadden Sea for plaice, flounder and sole
from 1979 to 2019 with less frequent observations in
recent years.
Larval immigration at Balgzand, as indicated by
the time of maximum (= peak) abundance, starts with
plaice, followed by flounder and finally by sole
(Fig. 5). In the 1980s, peak abundance of plaice
occurred at the end of April, followed by flounder at
the end of May and sole at the end of June. Over
time, peak abundance for plaice and flounder has
shifted and in recent years occurred about 1 mo ear-
lier for plaice and 1.5 mo earlier for flounder. For sole,
a similar shift occurred before 2000, but the time of
peak abundance has been stable since then. The
data are in line with the expectation that the recent
warming of the Dutch coastal zone has advanced lar-
val flatfish immigration in spring, especially of the
cold-water species.
4.2. Expectation 2: Effect of increased seawater
temperature on spatial distribution and growth
potential is species-specific
4.2.1. Spatial distribution
Settling flatfish larvae have species-specific habi-
tat and sediment preferences (Gibson & Robb 2000).
Newly settled flatfish larvae have been observed in
most of the Wadden Sea habitats, especially in inter-
tidal and subtidal areas (Kuipers 1977, Zijlstra et al.
1982, van der Veer & Witte 1993, Freitas et al. 2016).
Plaice larvae settle on a wide range of sediment
types in intertidal and subtidal areas between March
and mid-May (Kuipers 1977, Zijlstra et al. 1982, van
der Veer & Witte 1993, Jager et al. 1995). Flounder
larvae settle in relatively muddy areas at low salini-
ties, or in fresh water in rivers or canals (Berghahn
1984, van der Veer et al. 1991, Jager et al. 1995). Set-
tlement of sole larvae occurs more widely in coastal
areas, and within the Wadden Sea mainly in sandy
and muddy habitats (Rijnsdorp et al. 1992), with a
preference for finer sediments (Post et al. 2017). Dab
larvae settle mainly in coastal waters in the North
Sea, and the size range of 0-group dab observed
within the Wadden Sea indicates that they migrate
into the Wadden Sea after settlement (Bolle et al.
1994). This means that habitat use within the Wad-
den Sea differs among species, with juvenile plaice
and flounder using both intertidal and subtidal areas,
and sole and dab concentrating mainly in subtidal
areas.
Juvenile flatfish spatial distribution patterns have
changed over time. Until the 1990s, various age
groups of plaice and flounder could be found in inter-
tidal areas (van der Veer et al. 2011). Subsequently,
the densities of I- and II-group plaice in intertidal
areas decreased, and from 2000 onwards only 0-
group was observed. A similar pattern, though less
pronounced, was observed for juvenile flounder in
the intertidal areas (van der Veer et al. 2011). Simul-
taneously with the strong decreases in I- and II-
group plaice in intertidal areas, increased numbers
were observed in subtidal areas and tidal channels
(Freitas et al. 2016) and also in deeper waters outside
the Wadden Sea (van Keeken et al. 2007). Inside the
188

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning
Wadden Sea, settlement of 0-group plaice still occurs
in intertidal areas, but they move quickly to deeper
subtidal areas and tidal channels (Freitas et al. 2016).
It is not clear whether a similar shift in distribution to
deeper waters has also occurred for flounder and sole
(van der Veer et al. 1991, 2001).
The age composition of juvenile flatfish in the
Dutch Wadden Sea has also changed over time. In
the 1960s, 0-, I-, II- and III-group plaice were ob -
served (Fonds 1983). In the early 1980s, III-group dis-
appeared from the Wadden Sea. From the mid-1980s
onwards, densities of I- and II-group plaice also
decreased (van der Veer et al. 2011; Fig. 6). Since
2000, II-group has disappeared and densities of I-
group have been low (Fig. 6). For dab, a decline in all
age groups was observed from the 1990s onwards
(Tulp et al. 2008; Fig. 6). For flounder, the time series
is shorter and does not reveal any clear change in the
past 15 yr. For sole, a decrease in the density of I-
group occurred since the 1990s, but the pattern is
less clear than for plaice and dab (Fig. 6).
The changes in juvenile flatfish distribution pat-
terns and age composition in the Wadden Sea are
species-specific, and in line with the expectation.
189
ad
b
c
e
f
Day number
Peak abundance (ind. [103 m2]–1)
Fig. 5. Immigrating flatfish (plaice Pleuronectes platessa, flounder Platichthys flesus and sole Solea solea) larvae (just-settled
individuals ≤15 mm) at Balgzand as a proxy for larval immigration. Interannual pattern in time of peak abundance of just-
settled 0-group (a) plaice, (b) flounder and (c) sole in spring. Generalized additive model (GAM) with 95% confidence inter-
val; plaice R2adj = 0.34; p < 0.05; flounder R2adj = 0.43; p < 0.05; sole R2adj = 0.49; p < 0.05. Pattern in year-class strength of (d)
plaice, (e) flounder and (f) sole, as indicated by peak density during settlement. Data from the compilation in Jung et al. (2017)
and H. van der Veer & J. Witte (unpubl.) For more information, see van der Veer (1986) and Section 4.1

Mar Ecol Prog Ser 693: 183–201, 2022
The disappearance of the cold-water species with
their low temperature preference and tolerance sug-
gests a relationship with the increased seawater tem-
peratures in the Wadden Sea.
4.2.2. Growth
The species-specific temperature preference and
tolerance ranges (see Fig. 1 for explanation) can be
applied to the temperature conditions in the Wadden
Sea to determine the seasonal growth windows for
the various species. Daily seawater temperature
measurements from the NIOZ jetty in the Marsdiep
tidal inlet in the western Wadden Sea are available
from 1982 onwards, and were reconstructed for the
period 1956−1982. Specifically, SST data were taken
from 2 stations in the western Dutch Wadden Sea:
the NIOZ jetty and Breezanddijk. Daily SST meas-
urements were available from 1957 to 1989 for
Breezanddijk (https://waterinfo.rws.nl) and from
1982 to present for the NIOZ jetty (NIOZ unpubl.).
Data for the period 1982−1989 were used to deter-
mine the linear relationship between daily SST at
Breezanddijk and daily SST at the NIOZ jetty:
SSTMarsdiep = 0.91 × SSTBreezanddijk + 1.47 (R2 = 0.96; p <
0.001). This relationship was used to reconstruct daily
SST for the period 1956−1982 for the NIOZ jetty.
Classification of daily water temperatures for pref-
erence and tolerance of the 0-groups of the various
flatfish species during the growing season (1 April to
30 September) shows that in spring the temperatures
are within the tolerance limits of all flatfish species,
and do not restrict growth in any year (Fig. 7a). In
summer, the number of days with temperatures
within the respective preference ranges and below
the optimum temperatures (green in Fig. 7) de -
creased for 0-group plaice and dab, especially in the
last decades. For 0-group flounder, there was no
trend. For 0-group sole, a warm-water species, tem-
peratures were at the low end of the preference
range in spring and autumn (blue), and below the
optimum in summer (green).
For 0-group plaice and flounder, water tempera-
tures during the growing season remain within their
respective tolerance ranges, but they exceed the
optimum during parts of the summer. For 0-group
dab, water temperatures in summer exceed the toler-
ance range (red). The growth conditions during the
growing season improved over the years for 0-group
190
1970 1980 1990 2000 2010 2020
0
2
4
6
age.0 age.1 age.2plus
1970 1980 1990 2000 2010 2020
0
2
4
6
-1
4th root transformed density (n ha )
a
d
b
c
0
2
4
6
0
2
4
6
Fig. 6. Mean catch (fourth root transformed density of different age groups of juvenile (a) plaice, (b) dab, (c) sole and (d) floun-
der in the Demersal Fish Survey in the subtidal areas of the Dutch Wadden Sea in autumn. Data: Wageningen Marine
Research (unpubl.). Missing years for dab and flounder are due to missing age data

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning 191
Fig. 7. Classification of daily water temperature conditions for 0-group flatfish growth in the western Wadden Sea between
1956 and 2018, based on daily water temperature measurements in the Marsdiep. (a) Daily classification according to species-
specific tolerance range from 1956 to 2018 for the 4 species. Blue: low temperatures less than 10% maximum growth; green:
growth rates >10 % maximum growth until maximum growth at the optimal temperature; orange: growth range of tempera-
tures above optimal temperature until 10% maximum growth; red: high temperatures <10 % maximum growth. (b) Number
of green and orange days during the growing season (1 April to 30 September) for the 4 species. For more explanation,
see Fig. 1

Mar Ecol Prog Ser 693: 183–201, 2022
192
Location Year tmax Dmax M Days until Mt Reference
(ind. [10
3
m
2
]
−1
)
(d−1) 30 Sept
0-group plaice
Nordstrander 1981 145 70 0.002 125 0.250 Berghahn (1986) in: Iles & Beverton (1991)
Bay 1982 154 105 0.013 116 1.508 Berghahn (1986) in: Iles & Beverton (1991)
Mean 150 88 0.008 0.879
Dollard 1992 113 46 0.011 157 1.727 Jager et al. (1995)
Mean 113 46 0.011 1.727
Balgzand 1973 129 500 0.010 141 1.410 Kuipers (1977) in: Iles & Beverton (1991)
1975 122 137 148 Zijlstra et al. (1982) in: Iles & Beverton (1991)
1976 126 191 0.009 144 1.296 Zijlstra et al. (1982) in: Iles & Beverton (1991)
1977 88 202 0.007 182 1.274 Zijlstra et al. (1982) in: Iles & Beverton (1991)
1978 129 519 0.009 141 1.269 Zijlstra et al. (1982) in: Iles & Beverton (1991)
1979 121 320 0.008 149 1.192 Zijlstra et al. (1982) in: Iles & Beverton (1991)
1980 113 164 157 van der Veer (1986) in: Iles & Beverton (1991)
1981 126 360 0.025 144 3.600 van der Veer (1986) in: Iles & Beverton (1991)
1982 118 297 0.014 152 2.128 van der Veer (1986) in: Iles & Beverton (1991)
1993 117 370 0.034 153 5.202 van der Veer et al. (2000b)
1994 108 375 0.030 162 4.860 van der Veer et al. (2000b)
1995 94 244 0.029 176 5.104 van der Veer et al. (2000b)
1996 98 1282 0.021 172 3.612 van der Veer et al. (2000b)
1997 100 453 0.031 170 5.270 van der Veer et al. (2000b)
1998 91 262 0.026 179 4.654 van der Veer et al. (2000b)
1999 83 312 0.022 187 4.114 van der Veer et al. (2000b)
2000 94 674 H. van der Veer & J. Witte (unpubl.)
2001 125 760 H. van der Veer & J. Witte (unpubl.)
2002 63 324 H. van der Veer & J. Witte (unpubl.)
2007 85 379 H. van der Veer & J. Witte (unpubl.)
2009 90 216 H. van der Veer & J. Witte (unpubl.)
2014 93 582 H. van der Veer & J. Witte (unpubl.)
2019 87 379 H. van der Veer & J. Witte (unpubl.)
Mean 104 404 0.020 166 3.213
0-group flounder
Balgzand 1979 162 89 0.023 108 2.484 van der Veer et al. (1991)
1980 163 28 0.071 107 7.597 van der Veer et al. (1991)
1981 153 227 0.089 117 10.413 van der Veer et al. (1991)
1982 158 23 0.043 112 4.816 van der Veer et al. (1991)
1993 130 88 0.034 140 4.760 H. van der Veer & J. Witte (unpubl.)
1994 122 305 0.050 148 7.400 H. van der Veer & J. Witte (unpubl.)
1995 136 399 0.050 134 6.700 H. van der Veer & J. Witte (unpubl.)
1996 153 229 0.054 117 6.318 H. van der Veer & J. Witte (unpubl.)
1997 146 9 0.039 124 4.836 H. van der Veer & J. Witte (unpubl.)
1998
1999
2000 122 80 0.055 148 8.140 H. van der Veer & J. Witte (unpubl.)
2001 157 51 0.022 113 2.486 H. van der Veer & J. Witte (unpubl.)
2002
2007 113 51 0.035 157 5.495 H. van der Veer & J. Witte (unpubl.)
2009 139 13 0.006 131 0.786 H. van der Veer & J. Witte (unpubl.)
2014 121 36 0.016 149 2.384 H. van der Veer & J. Witte (unpubl.)
Mean 141 116 0.042 129 5.330
Dollard 1992 168 26 0.028 102 2.856 Jager et al. (1995)
Mean 168 26 0.028 2.856
0-group sole
Dollard 1992 224 4 0.011 46 0.506 Jager et al. (1995)
Mean 224 4 0.011 0.506
Table 1. Maximum densities, mortality rates of 0-group flatfish for various Wadden Sea nursery areas and years — Nordstrander
Bay, Germany (54° 28’ N, 8°47’ E); Dollard, The Netherlands (53°17’ N, 7° 07’E); Balgzand, The Netherlands (52° 54’N, 4° 91’ E).
tmax: time (d) of maximum observed density from 1 January; Dmax: maximum observed density; M: mean daily instantaneous
mortality rate based on the slope of the regression of densities over time; Mt: total stage mortality (M × number of days from peak
numbers until 30 September). For more information, see Beverton & Iles (1992). Empty cells: years with insufficient data

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning
sole (more days marked in green) (Fig. 7b).
In conclusion, the growth window in the
western Wadden Sea is becoming increas-
ingly unfavourable especially in summer
for 0-group dab, plaice and flounder, but not
for sole.
Based on an annual autumn survey (DFS)
in Dutch, German and Danish coastal waters,
Teal et al. (2008) did not find a clear trend in
the mean size at the end of the growing sea-
son for 0-group plaice, whereas for 0-group
sole, the mean size increased since the 1980s,
coinciding with the increase in seawater tem-
perature. Therefore, the effect of increased
seawater temperatures in the Wadden Sea on
growth appears to be species-specific and
depends on physiological preference, in
agreement with the expectation.
4.3. Expectation 3: Increased top predator
abundance and fisheries have increased
flatfish mortality
Mortality can be calculated from changes
in densities over time when immigration and
emigration can be determined or excluded.
Mortality is often expressed as an instanta-
neous daily mortality rate calculated from
the slope of a linear regression through log-
transformed observed local densities over
time (Beverton & Iles 1992).
Mortality estimates of 0-group flatfish species in
the Wadden Sea are available for only a few semi-
closed populations: for 0-group plaice (Zijlstra et al.
1982, van der Veer 1986, van der Veer et al. 2000b)
and flounder (van der Veer et al. 1991) in the Dutch
Wadden Sea in the Balgzand intertidal and for 0-
group plaice, flounder and sole in the Dollard (Jager
et al. 1995). For the North Frisian German Wadden
Sea, mortality estimates are available for a 0-group
plaice population in a mixed intertidal and subtidal
setting (Berghahn 1986); however, these estimates
also include shrimp fishery bycatch mortality in the
subtidal area.
Comparison of mortality rates from the various
intertidal areas and species showed a range from
0.002 to 0.034 d−1, including interannual variability
within and among species and areas (Table 1). The
largest amount of information is available for the
Balgzand intertidal area, where the mortality rate
increased for 0-group plaice between 1973 and 1999
(Fig. 8a). Furthermore, the increase in instantaneous
daily mortality rate of 0-group plaice correlated with
the increase in mean seawater temperature in the
Marsdiep in spring (Table 2), which suggests that
part of the increased mortality might be due to in -
creased seawater temperature conditions. Mortality
estimates could not be made for the last 2 decades
because of their earlier migration to deeper waters.
For 0-group flounder, instantaneous daily mortality
rates at the Balgzand intertidal area did not change
in time. On average, instantaneous daily mortality
rates of 0-group flounder were roughly twice those of
0-group plaice (Fig. 8b), reflecting the settlement of
flounder both at a smaller size and at a higher water
temperature later in the year (van der Veer 1986, van
der Veer et al. 1991). The instantaneous daily mortal-
ity rate of 0-group flounder did not correlate with the
increase in mean seawater temperature in the Mars-
diep in spring and summer (Table 2).
Shrimp fisheries are restricted to subtidal areas, so
there is no bycatch-induced mortality in intertidal
areas. Predation pressure by top predators has in -
creased strongly since the 1990s because of increased
193
0
0.01
0.02
0.03
0.04 0-group plaice
a
0
0.02
0.04
0.06
0.08 0-group flounder
1970 1980 1990 2000 2010 2020
Daily mortality (d
–1
)Daily mortality (d
–1
)
b
Fig. 8. Average daily instantaneous mortality among 0-group (a) plaice
and (b) flounder at the Balgzand intertidal. Note the differences in
the y-axis scales between the 2 species. For more information, see
Section 4.3 and Table 1

Mar Ecol Prog Ser 693: 183–201, 2022
abundance of cormorants, harbour seals and grey
seals (Fig. 9). The mean daily mortality of 0-group
plaice was significantly positively correlated to the
index of predation by top predators (Spearman’s
rank correlation: n = 14; rS = 0.71), in contrast to 0-
group flounder (n = 14; rS = −0.55).
The changes in daily mortality of 0-group plaice
are in agreement with the expectation that the
increase in abundance of top predators has increased
the mortality of juvenile flatfish in the Wadden Sea.
The results for 0-group flounder are not in line with
this expectation. The available data are not sufficient
to establish the contribution of bycatch-induced mor-
tality by shrimp fisheries.
4.4. Expectation 4: Year-class strength of cold-
water species will decrease in response to
increased seawater temperatures offshore
The peak abundance of settling flatfish larvae, used
as proxy for larval supply and 0-group at the
Balgzand intertidal, showed the highest densities for
plaice, followed by flounder and then sole throughout
the time series (Fig. 5). Large interannual variations
were observed in all 3 species. The temporal varia-
tions of the 3 species appeared to be similar, with re -
latively high peak densities in the 1990s, but there
were no significant relationships between year-class
strengths of the 3 species (plaice versus flounder and
sole: r2adj = 0.07; flounder versus sole: r2adj = 0.27).
Time series of recruitment to the North Sea fish
stocks are available for I-group plaice and sole from
1957 onwards and for dab from 2003 onwards (ICES
2017, 2018a,b). Recruitment estimates showed year-
to-year fluctuations, with exceptionally strong re-
cruitment of plaice in 1964, 1986 and 1997 and of sole
in 1959, 1964, 1988 and 1992. After the peak in 1986,
plaice recruitment decreased until 1992, and then sta-
bilized but with a tendency to increase again. Sole re-
cruitment did not change over time. Dab recruitment
increased strongly from 2003 to 2014, and then de-
creased in 2015 and 2016. The decreasing
trends for juvenile flatfish abundance in
autumn in the Wadden Sea (Fig. 5) were
not reflected in the recruitment estimates
(Fig. 10). The results do not support the
expectation that year-class strength of
plaice and other cold-water species de-
creases in response of the increase in sea-
water temperature offshore.
5. DISCUSSION
5.1. Shifts in flatfish nursery function
The early studies starting in the 1890s
(Petersen 1895, Redeke 1905, Johansen
194
Year TSP TSU TMEAN M (d−1)
(°C) (°C) (°C) Plaice Flounder
1973 8.2 17.6 12.9 0.01
1976 7.5 18.4 13.0 0.009
1977 8.1 16.2 12.2 0.007
1978 7.6 15.9 11.7 0.009
1979 6.6 16.4 11.5 0.008 0.023
1980 7.9 16.7 12.3 0.071
1981 8.7 16.6 12.6 0.025 0.089
1982 8.3 18.3 13.3 0.014 0.043
1993 9.0 16.8 12.9 0.034 0.034
1994 8.3 17.8 13.1 0.03 0.050
1995 8.7 18.1 13.4 0.029 0.050
1996 6.4 17.0 11.7 0.021 0.054
1997 8.7 18.4 13.5 0.031 0.039
1998 9.8 16.8 13.3 0.026
1999 10.0 18.2 14.1 0.022
2000 10.1 17.2 13.6 0.055
2001 8.5 18.1 13.3 0.022
2002 9.7 18.4 14.0
2003 9.3 19.2 14.2 0.035
2004 9.3 17.8 13.5 0.006
2005 8.3 17.0 12.7 0.016
Table 2. Mean water temperature in the Marsdiep in spring
(March−May; TSP), summer (June−August; TSU) and
March−August (TMEAN) together with mean instantaneous
mortality rate (M ) of 0-group plaice and flounder at Balg-
zand. Spearman rank correlations (rS) with p-values (ns: not
significant): Plaice: M−TSP: rS = 0.70, p < 0.01; M−TSU: rS =
0.36, ns; M−TMEAN: rS = 0.58, p < 0.05. Flounder: M−TSP:
rS = 0.11, ns; M−TSU: rS = 0.22, ns; M−TMEAN rS = 0.17, ns.
Empty cells: years with insufficient data
0
10
20
30
1960 1970 1980 1990 2000 2010 2020
Daily predation top predators
(tonnes WW d-1)
Fig. 9. Index of predation pressure by top predators in the Dutch Wadden
Sea. WW: wet weight. For more information and data sources, see van der
Veer et al. (2015a)

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning
1913, Lübbert 1925, Bückmann 1935a,b, Smidt 1951),
the systematic inventories in the western Wadden
Sea in 1963−1964 (Creutzberg & Fonds 1971, Fonds
1983), in 1986 (van der Veer & Witte 1993) and in
2009 (Freitas et al. 2016), the studies of the intertidal
Balgzand area in the 1970s (Kuipers 1977), the long-
term fyke catches since 1960 (van der Veer et al.
2015a) and the annual DFS since 1970 (Zijlstra 1972,
Tulp et al. 2008, this study) all show that until the
1980s, the Wadden Sea was a system with numerous
seasonally immigrating juvenile plaice, flounder,
sole and dab of different age groups.
From the 1970s onwards, the Wadden Sea has
experienced major changes. The western Wadden
Sea has become a system with higher and still
increasing seawater temperatures (van Aken 2010),
while returning to lower primary production
levels after a period of eutrophication in the
1980s (Jacobs et al. 2020), but nevertheless
with a higher intertidal macrozoobenthic bio-
mass (Beukema & Dekker 2020), higher num-
bers of top predators and an increased shrimp
fishery (van der Veer et al. 2015a). In the Jade
tidal basin in the German part of the Wadden
Sea, climate warming, decreasing nutrient loads
and species introductions occurred between
the 1970s and 2009 with resulting changes
in the macrofauna communities (Schückel &
Kröncke 2013) and with decreasing abun-
dances of juvenile plaice and dab while abun-
dances of juvenile sole in creased (Meyer et al.
2016). The functional changes for the western
Wadden Sea and Jade, caused by increased
water temperature and a eutrophication event,
are most likely indicative of changes in the
whole international Wadden Sea (see also
Kloepper et al. 2017).
Since the 1980s, the nursery function of the
Wadden Sea for flatfish species has changed
substantially, resulting in decreased suitability
for juvenile plaice and dab (Tulp et al. 2008,
van der Veer et al. 2011, Meyer et al. 2016,
ICES 2018c). The question is to what extent
these changes were caused by internal (local)
or external (large-scale) factors, and whether
they result from bottom-up or top-down regu-
lation. There are strong indications that in -
creased seawater temperature, both locally
and offshore, is an important causal factor. For
North Sea plaice, the timing of spawning is
negatively correlated with seawater tempera-
ture (Rijnsdorp 1989). For the Southern Bight
spawning population that supplies the Balg-
zand intertidal area with larvae (Harding & Talbot
1973, Talbot 1977, van der Veer et al. 1998, Bolle et
al. 2009), the observed trend of increasing sea water
temperatures in the coastal zone (van Aken 2008a) is
expected to cause earlier spawning, faster egg and
larval development, and earlier settling. In contrast,
Hovenkamp (1990) argued, based on RNA:DNA-
ratios and otolith growth rates, that plaice larvae
experience periods of food limitations causing
growth retention, which counteracts a faster devel-
opment. This agrees with smaller ob served reduc-
tions in development time than ex pected from labo-
ratory data (van der Veer et al. 2009). Nevertheless,
the peak in plaice larval immigration occurs about
1 mo earlier at the Balgzand intertidal compared to 4
decades ago. The similar trend in earlier immigration
195
0
1000
2000
3000
4000
5000 Plaice
Recruitment (millions)
0
200
400
600
800 Sole
Recruitment (millions)
0
0.4
0.8
1.2
1.6
2.0
1950 1960 1970 1980 1990 2000 2010 2020
Dab
Recruitment (relative index)
a
b
c
Fig. 10. Trends in recruitment to the fisheries of North Sea (a) plaice,
(b) sole and (c) dab, according to ICES (2017, 2018a,b)

Mar Ecol Prog Ser 693: 183–201, 2022
of flounder larvae suggests a relationship between
increased seawater temperatures, earlier timing of
spawning and shorter egg and larval development
times for these species.
Locally, increased seawater temperatures in the
Wadden Sea are expected to be a critical factor for
the observed changes in habitat use by and growth
performance of the various flatfish species. The
decrease in abundance of juvenile plaice and dab
from their 1980s levels (Tulp et al. 2008, van der Veer
et al. 2011, ICES 2018c) coincides with the start of the
increase in seawater temperatures (van Aken 2008a).
After the 1980s, seawater temperatures during the
growing season increasingly exceeded the optimum
for plaice, flounder and dab. Thermal limits are
thought to be caused by an increasing mismatch
between oxygen demand and the capacity of oxygen
supply to tissues, and has been suggested to cause
the decline of eelpout Zoarces viviparus in the Wad-
den Sea (Pörtner & Knust 2007). For sole, a warm-
water species, seawater temperatures are still within
their preferred temperature range. Increased water
temperatures may also cause the observed shifts in
habitat use. Shallow waters, such as intertidal areas,
warm up more quickly than deeper waters in sum-
mer (van der Veer & Bergman 1986), causing juve-
nile plaice and flounder to abandon the intertidal
areas earlier in the season.
As a result of the warming, summer seawater tem-
peratures in the Wadden Sea exceed the tolerance
range of juvenile dab, as well as the optimum for
juvenile plaice and flounder, but have improved con-
ditions for 0-group sole. Juvenile dab have vanished
almost completely from the Wadden Sea. Juvenile
plaice and flounder still grow up in the Wadden Sea,
but they increasingly use deeper waters. For juvenile
sole, the increased temperatures enhance growth
(Teal et al. 2008). In the adjacent North Sea, seawater
temperatures have increased by 0.2 to 0.6°C per
decade between 1980 and 2009 (Belkin 2009), posi-
tively affecting the growth potential of sole but also
plaice (Teal et al. 2012).
The period of eutrophication in the 1980s has been
suggested to have caused an increase in fish produc-
tion and a shift in the distributions of flatfishes.
Assuming that fish growth is food limited, Boddeke &
Hagel (1991) stated that the eutrophication of the
Dutch coastal zone caused enhanced production.
Inversely, the reduction in nutrient loads to the Wad-
den Sea reduced fish production, an effect also sug-
gested by Støttrup et al. (2017) for juvenile flatfish
abundance in Danish coastal waters. In the western
Wadden Sea, flatfish growth was not affected by
eutrophication. The pattern before, during and after
the period of eutrophication was the same: juvenile
flatfish growth appears to be optimal (for plaice,
flounder, sole) in spring and early summer, and lim-
ited in summer not only in the Wadden Sea but also
in other flatfish nurseries (Freitas et al. 2012, van der
Veer et al. 2016). Growth rates for 4 resident fish
species in the Wadden Sea (twaite shad Allosa fallax,
bull-rout Myoxocephalus scorpius, thick-lipped grey
mullet Chelon labrosus and eelpout) are even higher
at present than during the period of eutrophication
(Bolle et al. 2021).
The correlation of mortality of 0-group plaice in
inter tidal areas with the mean seawater temperature
in spring suggests contributions from increased pre-
dation by shrimps, crabs and fishes (van der Veer &
Bergman 1987b) at higher temperatures; however, in
that case a similar relationship for 0-group flounder
is expected. On the other hand, the lower daily mor-
tality for 0-group plaice at the Balgzand intertidal
area during the 1980s compared with the 1990s (this
study; Table 1) suggests that enhanced system pro-
ductivity in response to eutrophication in the 1980s
(Philippart et al. 2007) reduces predation pressure.
Most of the top predators strongly increased in abun-
dance since the 1990s and consume juvenile flat-
fishes. Cormorants were estimated to cause substan-
tial mortality during the period July−September in
the 1990s (Leopold et al. 1998). Since then, cormorant
numbers have increased (van der Veer et al. 2015a).
Year-class strength in marine flatfishes is con-
trolled in early life history in agreement with the
hypothesis postulated by Hjort (1914, 1926), through
a combination of density-independent processes
related to fluctuations in the physical environment
and density- dependent processes caused by either
predation or food competition (Leggett & DeBlois
1994, van der Veer et al. 2000a,b, 2015b, Beggs &
Nash 2007, Taylor et al. 2010). Various field and
hydrodynamic modelling studies demonstrated the
importance of hydrodynamic conditions in connect-
ing spawning grounds to nursery areas and causing
interannual fluctuations in larval supply to nursery
grounds (Harding & Talbot 1973, Talbot 1977, Hard-
ing et al. 1978, van der Veer et al. 1998, de Graaf et
al. 2004, Fox et al. 2006, Bolle et al. 2009, Erftemeijer
et al. 2009, Savina et al. 2010, Hufnagl et al. 2013,
Lacroix et al. 2013, Tiessen et al. 2014, Barbut et al.
2019, Cabral et al. 2021). Various studies also point to
negative relationships between seawater tempera-
tures and year-class strength. Van der Veer (1986)
and van der Veer & Witte (1999) observed an inverse
relationship between seawater temperatures during
196

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning
larval drift and the abundance of settling plaice lar-
vae at Balgzand. Such a negative relationship be -
tween sea water temperature in the first few months
of the year and subsequent year-class strength was
confirmed for most plaice stocks around the UK (Fox
et al. 2000) and several areas in the North Sea for
plaice and sole (Akimova et al. 2016). The expecta-
tion that year-class strength of plaice and other cold-
water species would decrease as a consequence of
the increase in sea water temperature offshore in the
North Sea (van Aken 2010) is so far not reflected in
the abundance of immigrating and settling larvae at
the Balgzand intertidal.
5.2. Future perspectives
Most climate change studies predict increases in
sea level and water temperature for the North Sea,
alongside decreases in salinity and primary produc-
tion, with regional differences and uncertainties in
estimates of both magnitudes and consequences for
hydrodynamic circulation (Schrum et al. 2016). For
the Wadden Sea, a further rise in sea level (Ver-
meersen et al. 2018) and an increase in atmospheric
temperatures by 1 to 5°C towards the end of the 21st
century is predicted (Oost et al. 2017). Rijnsdorp et al.
(2009) predicted a general (further) shift in abun-
dance and distribution with latitude and depth for
marine species and suggested that the response of
demersal species, including flatfishes, may be ham-
pered by geographically fixed habitats, such as nurs-
ery areas. However, spawning adults and embryos
appear to be the most vulnerable life stages to cli-
mate warming due to their narrower temperature tol-
erance ranges (Dahlke et al. 2020). This means that
further climate change may especially affect spawn-
ing in the open sea (see also the CERES project:
https://ceresproject.eu). Until the mid-2000s, the
increase in temperatures of coastal waters by 1.5°C
(van Aken 2008a) did not change larval plaice set-
tling at the Balgzand intertidal area. The broad spa-
tial distribution of plaice in the North Sea, with
spawning grounds in the English Channel, Southern
Bight and German Bight, may provide potential for
the Balgzand nursery and other areas of the Wadden
Sea to shift to larvae from other spawning areas in
the future.
Nursery use in the Dutch Wadden Sea has de -
creased over time especially for plaice and dab. This
trend will likely continue with the predicted in crease
in seawater temperatures. However, at present, the
Wadden Sea is still an important area for juvenile
flatfish. Furthermore, the area is still within the toler-
ance limits of juvenile dab in autumn and winter,
when temperatures are lower. Moreover, species
with a high temperature tolerance and optimum,
such as the tub gurnard Chelidonichthys lucerna,
can benefit from the higher temperatures (Tulp et al.
2017).
The distribution of juvenile and adult plaice has
shifted to deeper and northern areas in the North Sea,
most likely in response to climate change (warming)
(van Keeken et al. 2007, Engelhard et al. 2011). Fur-
ther climate change will reduce the ‘temperature
window’ for the remaining age groups of the cold-
water species in the Wadden Sea (plaice, dab and to
a lesser extent flounder), and growing conditions in
late spring and summer will become less favourable
as temperatures exceed their respective thermal tol-
erance range. Only sole can cope with higher water
temperatures. However, other, new Lusitanian (warm-
water) fish species may settle in the Wadden Sea as
water temperatures increase.
The nursery function of the Wadden Sea will con-
tinue to change, and suitable nursery areas will shift
towards the coastal zone in the North Sea, in agree-
ment with expectations that habitat availability for
North Sea plaice will reduce with further climate
change (Petitgas et al. 2013). However, so far the
decreasing abundances of juvenile plaice and dab in
the Wadden Sea have not changed recruitment esti-
mates for the North Sea, suggesting that the juve-
niles of these species have apparently found other
alternative nursery areas.
Acknowledgements. We thank all students, assistants and
crew members from NIOZ and WMR who assisted in collect-
ing the field data throughout the years, and especially
Sieme Gieles, Marco Kortenhoeven and Ewout Adriaans
from NIOZ and Marcel de Vries, Andre Dijkman, Gerrit
Rink and Thomas Pasterkamp from WMR. We also thank
Joan van der Molen for correcting the English text. The DFS
is carried out as part of the statutory tasks set out in Dutch
legislation on fisheries management, financed by the Dutch
Ministry of Economic Affairs.
LITERATURE CITED
Aarts G, Brasseur S, Poos JJ, Schop J and others (2019) Top-
down pressure on a coastal ecosystem by harbor seals.
Ecosphere 10: e02538
Akimova A, Núñez-Riboni I, Kempf A, Taylor MH (2016)
Spatially-resolved influence of temperature and salinity
on stock and recruitment variability of commercially im -
portant fishes in the North Sea. PLOS ONE 11: e0161917
Augley J, Huxham M, Fernandes TF, Lyndon AR (2008) The
effect of salinity on growth and weight loss of juvenile
plaice (Pleuronectes platessa, L): an experimental test.
J Sea Res 60: 292−296
197

Mar Ecol Prog Ser 693: 183–201, 2022
Barbut L, Crego CG, Delerue-Ricard S, Vandamme S, Vol-
ckaert FAM, Lacroix G (2019) How larval traits of six flat-
fish species impact connectivity. Limnol Oceanogr 64:
1150−1171
Beck MW, Heck KL, Able KW, Childers DL and others
(2001) The identification, conservation, and manage-
ment of estuarine and marine nurseries for fish and
invertebrates. Bioscience 51: 633−641
Beggs SE, Nash RDM (2007) Variability in settlement and
recruitment of 0-group dab Limanda limanda L. in Port
Erin Bay, Irish Sea. J Sea Res 58: 90−99
Belkin IM (2009) Rapid warming of large marine ecosys-
tems. Prog Oceanogr 81: 207−213
Berghahn R (1984) Zeitliche und räumliche Koexistenz aus-
gewählter Fisch- und Krebsarten im Wattenmeer unter
Berücksichtigung von Räuber−Beute-Beziehungen und
Nahrungskonkurrenz. PhD dissertation, University of
Hamburg
Berghahn R (1986) Determining abundance, distribution,
and mortality of 0-group plaice (Pleuronectes platessa L.)
in the Wadden Sea. J Appl Ichthyol 2: 11−22
Bergman MJN, van der Veer HW, Zijlstra JJ (1988) Plaice
nurseries: effects on recruitment. J Fish Biol 33(Suppl A):
201−218
Beukema JJ, Dekker R (2020) Half a century of monitoring
macrobenthic animals on tidal flats in the Dutch Wadden
Sea. Mar Ecol Prog Ser 656: 1−18
Beverton RJH, Iles TC (1992) Mortality rates of 0-group
plaice (Pleuronectes platessa L.), dab (Limanda limanda
L.) and turbot (Scophthalmus maximus L.) in European
waters. II. Comparison of mortality rates and construc-
tion of life table for 0-group plaice. Neth J Sea Res 29:
49−59
Boddeke R, Hagel P (1991) Eutrophication of the North Sea
continental zone, a blessing in disguise. C.M. 1991/E: 7.
ICES, Copenhagen
Bolle LJ, Dapper R, Witte JIJ, van der Veer HW (1994) Nurs-
ery grounds of dab (Limanda limanda L.) in the southern
North Sea. Neth J Sea Res 32: 299−307
Bolle LJ, Dickey-Collas M, van Beek JKL, Erftemeijer PLA,
Witte JIJ, van der Veer HW, Rijnsdorp AD (2009) Vari-
ability in transport of fish eggs and larvae. III. Effects of
hydrodynamics and larval behaviour on recruitment in
plaice. Mar Ecol Prog Ser 390: 195−211
Bolle LJ, Hoek R, Pennock I, Poiesz SSH and others (2021)
No evidence for reduced growth in resident fish species
in the era of de-eutrophication in a coastal area in NW
Europe. Mar Environ Res 169: 105364
Böttcher ME, Oelschläger B, Höpner T, Brumsack HJ, Rul-
lkötter J (1998) Sulfate reduction related to the early dia-
genetic degradation of organic matter and ‘black spot’
formation in tidal sandflats of the German Wadden Sea
(southern North Sea): stable isotope (13C, 34S, 18O) and
other geochemical results. Org Geochem 29: 1517−1530
Brander K, Houghton RG (1982) Predicting the recruitment
of North Sea plaice from egg surveys. C.M. 1982/G: 5.
ICES, Copenhagen
Bückmann A (1935a) Untersuchungen über die Natur -
geschichte der Seezunge, die Seezungenbevölkerung
und den Seezungenfang in der Nordsee. Ber Dt Wiss
Komm Meeresforsch 7: 49−114
Bückmann A (1935b) Über die Jungschollenbevölkerung
der deutschen Wattenküste der Nordsee. Ber Dt Wiss
Komm Meeresforsch 7: 205−213
Cabral H, Drouineau H, Teles-Machado A, Pierre M and
others (2021) Contrasting impacts of climate change on
connectivity and larval recruitment to estuarine nursery
areas. Prog Oceanogr 196: 102608
Creutzberg F, Fonds M (1971) The seasonal variation in the
distribution of some demersal fish species in the Dutch
Wadden Sea. Thalassia Jugosl 7: 13−23
Dahlke FT, Wohlrab S, Butzin M, Pörtner HO (2020) Ther-
mal bottlenecks in the life cycle define climate vulnera-
bility of fish. Science 369: 65−70
de Graaf M, Jager Z, Vreugdenhil CB, Elorche M (2004)
Numerical simulations of tidally cued vertical migrations
of flatfish larvae in the North Sea. Estuar Coast Shelf Sci
59: 295−305
Engelhard GH, Pinnegar JK, Kell LT, Rijnsdorp AD (2011)
Nine decades of North Sea sole and plaice distribution.
ICES J Mar Sci 68: 1090−1104
Erftemeijer PLA, van Beek JKL, Bolle LJ, Dickey-Collas M,
Los HFJ (2009) Variability in transport of fish eggs and
larvae. I. Modelling the effects of coastal reclamation.
Mar Ecol Prog Ser 390: 167−181
Fonds M (1979) Laboratory observations on the influence of
temperature and salinity on development of the eggs and
growth of the larvae of Solea solea (Pisces). Mar Ecol
Prog Ser 1: 91−99
Fonds M (1983) The seasonal distribution of some fish spe-
cies in the western Dutch Wadden Sea. In: Wolff WJ (ed)
Ecology of the Wadden Sea. Balkema Press, Rotterdam,
p 5/42−5/77
Fonds M, Rijnsdorp AD (1988) Eten and groeien. In: Osse
JWM, Zijlstra JJ, van Emden HM (eds) Als een vis in the
water. Pudoc, Wageningen, p 120−138
Fonds M, Cronie R, Vethaak AD, van der Puyl P (1992)
Metabolism, food consumption and growth of plaice
(Pleuronectes platessa) and flounder (Platichthys flesus)
in relation to fish size and temperature. Neth J Sea Res
29: 127−143
Fox CJ, Planque BP, Darby CD (2000) Synchrony in the
recruitment time-series of plaice (Pleuronectes platessa
L) around the United Kingdom and the influence of sea
temperature. J Sea Res 44: 159−168
Fox CJ, McCloghrie P, Young EF, Nash RDM (2006) The
importance of individual behaviour for successful settle-
ment of juvenile plaice (Pleuronectes platessa L.): a mod-
elling and field study in the eastern Irish Sea. Fish
Oceanogr 15: 301−313
Freitas V, Cardoso JFMF, Peck MA, Kooijman SALM, van
der Veer HW (2010) Analysis of physiological perform-
ance of North Atlantic marine organisms by means of
interspecies differences in DEB parameters. Phil Trans R
Soc B 365:3553– 3565
Freitas V, Kooijman SALM, van der Veer HW (2012) Latitu-
dinal trends in habitat quality of shallow-water flatfish
nurseries. Mar Ecol Prog Ser 471: 203−214
Freitas V, Witte JIJ, Tulp I, van der Veer HW (2016) Subtidal
areas replacing intertidal flats as the main nursery habi-
tat for plaice Pleuronectes platessa L. in the western
Wadden Sea. J Sea Res 111: 65−75
Frölicher TL, Laufkötter C (2018) Emerging risks from
marine heat waves. Nat Commun 9: 650
Fry FEJ (1971) The effect of environmental factors on the
physiology of fish. In: Hoar WS, Randall DJ (eds) Fish
physiology, Vol 6. Academic Press, New York, NY,
p 1−98
Gibson RN, Robb L (2000) Sediment selection in juvenile
plaice and its behavioural basis. J Fish Biol 56: 1258−1275
198

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning
Glorius S, Craeymeersch J, van der Hammen T, Rippen A
and others (eds) (2015) Effecten van garnalenvisserij in
Natura 2000 gebieden. IMARES Report C013/15
Harding D, Talbot JW (1973) Recent studies on the eggs and
larvae of the plaice (Pleuronectes platessa L.) in the
Southern Bight. Rapp P-V Réun Cons Perm Int Explor
Mer 164: 261−269
Harding D, Nicols JH, Tungate DS (1978) The spawning of
the plaice (Pleuronectes platessa) in the southern North
Sea and English Channel. Rapp P-V Réun Cons Perm Int
Explor Mer 172: 261−296
Heessen HJL, Daan N, Ellis JR (2015) Fish atlas of the Celtic
Sea, North Sea and Baltic Sea. Based on international
research-vessel surveys. Wageningen Academic Pub-
lishers & KNNV Publishing, Wageningen
Hiddink JG (1997) Experimental investigations on the effect
of temperature on egg production, larval quality and
recruitment in flatfish. NIOZ-Rapport 1997-4. Nether-
lands Institute for Sea Research, Marine Ecology, Den
Burg
Hjort J (1914) Fluctuations in the great fisheries of Northern
Europe viewed in the light of biological research. Rapp
P-V Réun Cons Perm Int Explor Mer 20: 1−228
Hjort J (1926) Fluctuations in the year classes of important
food fishes. J Cons Int Explor Mer 1: 5−38
Hovenkamp F (1990) Growth differences in larval plaice
Pleuronectes platessa in the Southern Bight of the North
Sea as indicated by otolith increments and RNA/DNA
ratios. Mar Ecol Prog Ser 58: 205−215
Hufnagl M, Peck MA, Nash RDM, Pohlmann T, Rijnsdorp
AD (2013) Changes in potential North Sea spawning
grounds of plaice (Pleuronectes platessa L.) based on
early life stage connectivity to nursery habitats. J Sea Res
84: 26−39
ICES (2017) Dab (Limanda limanda) in Subarea 4 and Division
3.a (North Sea, Skagerrak and Kattegat). ICES Advice on
fishing opportunities, catch, and effort. Greater North
Sea Ecoregion. ICES, Copenhagen
ICES (2018a) Plaice (Pleuronectes platessa) in Subarea 4
(North Sea) and Subdivision 20 (Skagerrak). ICES Advice
on fishing opportunities, catch, and effort. Greater North
Sea Ecoregion. ICES, Copenhagen
ICES (2018b) Sole (Solea solea) in Subarea 4 (North
Sea). ICES Advice on fishing opportunities, catch, and
effort. Greater North Sea Ecoregion. Version 3. ICES,
Copenhagen
ICES (2018c) Report of the Working Group on Beam
Trawl Surveys (WGBEAM). CM 2018/EOSG: 05. ICES,
Copenhagen
Iles TC, Beverton RJH (1991) Mortality rates of 0-group
plaice (Pleuronectes platessa L.), dab (Limanda limanda
L.) and turbot (Scophthalmus maximus L.) in European
waters: I. Statistical analysis of the data and estimation of
parameters. Neth J Sea Res 27:217–235
Jackson JBC, Kirby MX, Berger WH, Bjorndal KA and oth-
ers (2001) Historical overfishing and the recent collapse
of coastal ecosystems. Science 293: 629−637
Jacobs P, Kromkamp JC, van Leeuwen SM, Philippart CJM
(2020) Planktonic primary production in the western
Dutch Wadden Sea. Mar Ecol Prog Ser 639: 53−71
Jager Z, Kleef HL, Tydeman P (1995) Mortality and growth
of 0-group flatfish in the brackish Dollard (Ems estuary,
Wadden Sea). Neth J Sea Res 34: 119−129
Johansen AC (1913) Contributions to the biology of plaice
with special regard to the Danish plaice-fishery. VI. On
the immigration of plaice to the coastal grounds and
fjords on the west coast of Jutland. Medd Komm Havun-
ders Fisk 4: 1−26
Jung AS, Dekker R, Germain M, Philippart CJM, Witte JIJ,
van der Veer HW (2017) Long-term shifts in intertidal
predator and prey communities in the Wadden Sea and
consequences for food requirements and supply. Mar
Ecol Prog Ser 579: 37−53
Kloepper S, Baptist MJ, Bostelmann A, Busch JA and others
(eds) (2017) Wadden Sea Quality Status Report (2017).
Common Wadden Sea Secretariat, Wilhelmshaven.
https://qsr.waddensea-worldheritage.org
Kuipers BR (1977) On the ecology of juvenile plaice on a
tidal flat in the Wadden Sea. Neth J Sea Res 11: 56−91
Lacroix G, Maes GE, Bolle LJ, Volkaert FAM (2013) Model-
ling dispersal dynamics of the early life stages of a mar-
ine flatfish (Solea solea L.). J Sea Res 84: 13−25
Lefrançois C, Claireaux G (2003) Influence of ambient oxy-
genation and temperature on metabolic scope and scope
for heart rate in the common sole Solea solea. Mar Ecol
Prog Ser 259: 273−284
Leggett WC, DeBlois EM (1994) Recruitment in marine
fishes: Is it regulated by starvation and regulation in the
egg and larval stages? Neth J Sea Res 32:
119−134
Leopold MF, van Damme CJG, van der Veer HW (1998) Diet
of cormorants and the impact of cormorant predation on
juvenile flatfish in the Dutch Wadden Sea. J Sea Res 40:
93−107
Levin LA, Boesch DF, Covich A, Dahm C and others (2001)
The function of marine critical transition zones and the
importance of sediment biodiversity. Ecosystems 4:
430−451
Lotze HK (2005) Radical changes in the Wadden Sea fauna
and flora over the last 2,000 years. Helgol Mar Res 59:
71−83
Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH and oth-
ers (2006) Depletion, degradation, and recovery poten-
tial of estuaries and coastal seas. Science 312: 1806−1809
Lozán JL, Breckling P, Fonds M, Krog C, van der Veer HW,
Witte JIJ (1994) Uber die Bedeutung des Wattenmeeres
für die Fischfauna und deren regionale Veränderung. In:
Lozán JL, Rachor E, Reise K, von Westernhagen H, Lenz
W (eds) Warnsignale aus dem Wattenmeer. Blackwell
Wissenschafts Verlag, Berlin, p 226–234
Lübbert H (1925) Beobachtungen über den Schollenbestand
im Amerikahafen zu Cuxhaven im Jahre 1922. Ber Dt
Wiss Komm Meeresforsch 1: 294– 304
Malzahn AM, Clemmesen C, Wiltshire KH, Laakmann S,
Boersma M (2007) Comparative nutritional condition of
larval dab Limanda limanda and lesser sandeel Ammo -
dytes marinus in a highly variable environment. Mar
Ecol Prog Ser 334: 205−212
Meyer J, Kröncke I, Bartholomä A, Dippner JW, Schückel U
(2016) Long-term changes in species composition of
demersal fish and epibenthic species in the Jade area
(German Wadden Sea/Southern North Sea) since 1972.
Estuar Coast Shelf Sci 181: 284−293
Neill WH, Miller JM, van der Veer HW, Winemiller KO
(1994) Ecophysiology of marine fish recruitment: a con-
ceptual framework for understanding interannual vari-
ability. Neth J Sea Res 32: 135−152
Neira C, Rackemann M (1996) Black spots produced by
buried macroalgae in intertidal sandy sediments of the
Wadden Sea: effects on the meiobenthos. J Sea Res 36:
153−170
199

Mar Ecol Prog Ser 693: 183–201, 2022
Oost AP, Hofstede J, Weisse R, Baart F, Janssen G, Zijlstra R
(2017) Climate change. In: Kloepper S, Baptist MJ,
Bostelmann A, Busch JA and others (eds) Wadden Sea
Quality Status Report 2017. Common Wadden Sea Sec-
retariat, Wilhelmshaven. https://qsr.waddensea-world-
heritage.org/geomorphology-and-climate (Climate change;
accessed 12 Feb 2020)
Pauly D, Pullin RSV (1988) Hatching time in spherical,
pelagic, marine fish eggs in response to temperature and
egg size. Environ Biol Fishes 22: 261−271
Petersen CGJ (1895) The yearly immigration of young plaice
in the Limfjord from the German sea. Rep Dan Biol Stn 6:
1−48
Petitgas P, Rijnsdorp AD, Dickey-Collas M, Engelhard GH
and others (2013) Impacts of climate change on the com-
plex life cycles of fish. Fish Oceanogr 22: 121−139
Philippart CJM, Beukema JJ, Cadée CG, Dekker R and
others (2007) Impacts of nutrient reduction on coastal
communities. Ecosystems 10: 96−119
Poiesz SSH, Witte JIJ, van der Veer HW (2020) Only a few
key prey species fuel a temperate coastal fish food web.
Mar Ecol Prog Ser 653: 153−166
Pörtner HO, Knust R (2007) Climate change affects marine
fishes through the oxygen limitation of thermal toler-
ance. Science 315: 95−97
Post MHM, Blom E, Chen C, Bolle LJ, Baptist MJ (2017)
Habitat selection of juvenile sole (Solea solea L.): conse-
quences for shoreface nourishment. J Sea Res 122: 19−24
Rauck G, Zijlstra JJ (1978) On the nursery aspects of the
Waddensea for some commercial fish species and possi-
ble long-term changes. Rapp P-V Réun Cons Int Perm
Explor Mer 172: 266−275
Redeke HC (1905) The distribution of the plaice on the
Dutch coast. Rapp P-V Réun Int Perm Explor Mer
5(Appendix H): 1−10
Rijnsdorp AD (1989) Maturation of male and female North
Sea plaice (Pleuronectes platessa L.). J Cons Int Explor
Mer 46: 35−51
Rijnsdorp AD, van Beek FA, Flatman S, Millner RM, Riley
JD, Giret M, de Clerck R (1992) Recruitment of sole
stocks Solea solea (L.) in the Northeast Atlantic. Neth J
Sea Res 29: 173−192
Rijnsdorp AD, Peck MA, Engelhard GH, Möllmann C, Pin-
negar JK (2009) Resolving the effect of climate change
on fish populations. ICES J Mar Sci 66: 1570−1583
Ryland JS, Nichols JH, Sykes AM (1975) Effect of tempera-
ture on the embryonic development of the plaice, Pleu-
ronectes platessa L. (Teleostei). J Exp Mar Biol Ecol 18:
121−137
Savina M, Lacroix G, Ruddick K (2010) Modelling the trans-
port of common sole larvae in the southern North Sea:
influence of hydrodynamics and larval vertical move-
ments. J Mar Syst 81: 86−98
Schrum C, Lowe J, Meier HEM, Grabemann I and others
(2016) Projected change —North Sea. In: Quante M, Col-
ijn F (eds) North Sea region climate change assessment.
Springer Open, p 175−217
Schückel U, Kröncke I (2013) Temporal changes in intertidal
macrofauna communities over eight decades: a result of
eutrophication and climate change. Estuar Coast Shelf
Sci 117: 210−218
Smidt ELB (1951) Animal production in the Danish Wad-
densea. Meddr Komm Danm Fisk Havunders 11:1– 51
Støttrup JC, Munk P, Kodama M, Stedmon C (2017)
Changes in distributional patterns of plaice Pleuronectes
platessa in the central and eastern North Sea; do declin-
ing nutrient loadings play a role? J Sea Res 127: 164−172
Talbot JW (1977) The dispersal of plaice eggs and larvae in
the Southern Bight of the North Sea. J Cons Int Explor
Mer 37: 221−248
Taylor JC, Miller JM, Pietrafesa LJ, Dickey DA, Ross SW
(2010) Winter winds and river discharge determine juve-
nile southern flounder (Paralichthys lethostigma) recruit-
ment and distribution in North Carolina estuaries. J Sea
Res 64: 15−25
Teal LR, de Leeuw JJ, van der Veer HW, Rijnsdorp AD
(2008) Effects of climate change on growth of 0-group
sole and plaice. Mar Ecol Prog Ser 358: 219−230
Teal LR, van Hal R, van Kooten T, Ruardy P, Rijnsdorp AD
(2012) Bio-energetics underpins the spatial response of
North Sea plaice (Pleuronectes platessa L.) and sole
(Solea solea L.) to climate change. Glob Change Biol 18:
3291−3305
Tiessen MCH, Fernard L, Gerkema T, van der Molen J,
Ruardij P, van der Veer HW (2014) Numerical modelling
of physical processes governing larval transport in the
southern North Sea. Ocean Sci 10: 357−376
Tulp I, Bolle LJ, Rijnsdorp AD (2008) Signals from the shal-
lows: in search of common patterns in long-term trends
in Dutch estuarine and coastal fish. J Sea Res 60: 54−73
Tulp I, Bolle LJ, Meesters E, de Vries P (2012) Brown shrimp
abundance in northwest European coastal waters from
1970 to 2010 and potential causes for contrasting trends.
Mar Ecol Prog Ser 458: 141−154
Tulp I, van der Veer HW, Walker PA, van Walraven L, Bolle
LJ (2017) Can guild- or site-specific contrasts in trends or
phenology explain the changed role of the Dutch Wad-
den Sea for fish? J Sea Res 127: 150−163
van Aken HM (2008a) Variability of the salinity in the west-
ern Wadden Sea on tidal to centennial time scales. J Sea
Res 59: 121−132
van Aken HM (2008b) Variability of the water temperature
in the western Wadden Sea on tidal to centennial time
scales. J Sea Res 60: 227−234
van Aken HM (2010) Meteorological forcing of long-term
temperature variations of the Dutch coastal waters. J Sea
Res 63: 143−151
van Beek FA, Rijnsdorp AD, de Clerck R (1989) Monitoring
juvenile stocks of flatfish in the Wadden Sea and the
coastal areas of the southeastern North Sea. Helgol
Meeresunters 43: 461−477
van der Hammen T, Steenbergen J, van der Weide B (2015)
Deelrapport I: bijvangst. In: Glorius S, Craeymeersch K,
van der Hammen T, Rippen A and others (eds) Effecten
van garnalenvisserij in Natura 2000 gebieden. IMARES
Report C013/15, p 25−56
van der Meer J, Dankers N, Ens B, van Stralen M, Troost K,
Waser AM (2019) The birth, growth and death of inter-
tidal soft-sediment bivalve beds: no need for large-scale
restoration programs in the Dutch Wadden Sea. Ecosys-
tems 22: 1024−1034
van der Veer HW (1986) Immigration, settlement, and den-
sity-dependent mortality of a larval and early postlarval
0-group plaice (Pleuronectes platessa) population in the
western Wadden Sea. Mar Ecol Prog Ser 29: 223−236
van der Veer HW, Bergman MJN (1986) Development of
tidally related behaviour of a newly settled 0-group
plaice (Pleuronectes platessa) population in the western
Wadden Sea. Mar Ecol Prog Ser 31: 121−129
van der Veer HW, Bergman MJN (1987a) The nursery func-
200

van der Veer et al.: Changes in Wadden Sea flatfish nursery functioning
tion of the western Wadden Sea. In: Tougaard S, Asbirk
S (eds) Proc 5th International Wadden Sea Symposium
Esbjerg, 1986. Fiskeri-og Sofortmuseet, Soitvandsakvari-
ets, p 123−145
van der Veer HW, Bergman MJN (1987b) Predation by crus-
taceans on a newly settled 0-group plaice Pleuronectes
platessa population in the western Wadden Sea. Mar
Ecol Prog Ser 35: 203−215
van der Veer HW, Witte JIJ (1993) The ‘maximum growth/
optimal food condition’ hypothesis, a test for 0-group
plaice Pleuronectes platessa in the Dutch Wadden Sea.
Mar Ecol Prog Ser 101: 81−90
van der Veer HW, Witte JIJ (1999) Year-class strength of
plaice Pleuronectes platessa in the Southern Bight of the
North Sea: a validation and analysis of the inverse rela-
tionship with winter seawater temperature. Mar Ecol
Prog Ser 184: 245−257
van der Veer HW, van Raaphorst W, Bergman MJN (1989)
Eutrophication of the Dutch Wadden Sea, external nutri-
ent loadings of the Marsdiep and Vliestroom basins.
Helgol Meeresunters 43: 501−515
van der Veer HW, Bergman MJN, Dapper R, Witte JIJ (1991)
Population dynamics of an intertidal 0-group flounder
Platichthys flesus population in the western Dutch Wad-
den Sea. Mar Ecol Prog Ser 73: 141−148
van der Veer HW, Ruardy P, van den Berg AJ, Ridderinkhof
H (1998) Impact of interannual variability in hydrody-
namic circulation on egg and larval transport of plaice
Pleuronectes platessa L. in the southern North Sea. J Sea
Res 39: 29−40
van der Veer HW, Berghahn R, Miller JM, Rijnsdorp AD
(2000a) Recruitment in flatfish, with special emphasis on
North Atlantic species: progress made by the Flatfish
Symposia. ICES J Mar Sci 57: 202−215
van der Veer HW, Geffen AJ, Witte JIJ (2000b) Exception-
ally strong year classes in plaice Pleuronectes platessa:
Are they generated during the pelagic stage only, or also
in the juvenile stage? Mar Ecol Prog Ser 199: 255−262
van der Veer HW, Dapper R, Witte JIJ (2001) The nursery
function of the intertidal areas in the western Wadden
Sea for 0-group sole Solea solea (L.). J Sea Res 45: 271−279
van der Veer HW, Bolle LJ, Geffen AJ, Witte JIJ (2009) Vari-
ability in transport of fish eggs and larvae. IV. Interan-
nual variability in larval stage duration of immigrating
plaice in the Dutch Wadden Sea. Mar Ecol Prog Ser 390:
213−223
van der Veer HW, Koot J, Aarts G, Dekker R, Diderich W,
Freitas V, Witte JIJ (2011) Long term trends in juvenile
flatfish indicate a dramatic reduction in nursery function
of the Balgzand intertidal, Dutch Wadden Sea. Mar Ecol
Prog Ser 434: 143−154
van der Veer HW, Dapper R, Henderson PA, Jung AS,
Philippart CJM, Witte JIJ, Zuur AF (2015a) Changes over
50 years in fish fauna of a temperate coastal sea: degra-
dation of trophic structure and nursery function. Estuar
Coast Shelf Sci 155: 156−166
van der Veer HW, Freitas V, Leggett WC (2015b) Recruit-
ment level and variability. In: Gibson RN, Nash RDM,
Geffen AJ, van der Veer HW (Eds) Flatfishes. Biology
and exploitation. Fish and Aquatic Resources Ser 9.
Blackwell, Oxford, p 185−206
van der Veer HW, Jung AS, Freitas V, Philippart CJM, Witte
JIJ (2016) Possible causes for growth variability and sum-
mer growth reduction in juvenile plaice Pleuronectes
platessa L. in the western Dutch Wadden Sea. J Sea Res
111: 97−106
van Keeken OA, van Hoppe M, Grift RE, Rijnsdorp AD
(2007) Changes in the spatial distribution of North Sea
plaice (Pleuronectes platessa) and implications for fish-
eries management. J Sea Res 57: 187−197
van Raaphorst W, de Jonge VN (2004) Reconstruction of the
total N and P inputs from the IJsselmeer into the western
Wadden Sea between 1935−1998. J Sea Res 51: 109−131
Vermeersen BLA, Slangen ABA, Gerkema T, Baart F and
others (2018) Sea-level change in the Dutch Wadden
Sea. Neth J Geosci 97: 79−127
Willmer P, Stone G, Johnston I (2000) Environmental physi-
ology of animals. Blackwell Science, Oxford
Zijlstra JJ (1972) On the importance of the Waddensea as a
nursery area in relation to the conservation of the south-
ern North Sea fishery resources. Symp Zool Soc Lond 29:
233−258
Zijlstra JJ, Dapper R, Witte JIJ (1982) Settlement, growth
and mortality of postlarval plaice (Pleuronectes platessa
L.) in the western Wadden Sea. Neth J Sea Res 15:
250−272
201
Editorial responsibility: Konstantinos Stergiou, Thessaloniki,
Greece; Christine Paetzold, Oldendorf/Luhe, Germany
Reviewed by: 3 anonymous referees
Submitted: August 30, 2021
Accepted: May 12, 2022
Proofs received from author(s): July 15, 2022