Estuarine, Coastal and Shelf Science 85 (2009) 247256

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Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier.com/locate/ecss

Seasonal changes in community composition and trophic structure of sh

populations of ve salt marshes along the Essex coastline, United Kingdom
Benjamin C. Green*, David J. Smith, Sarah E. Earley, Leanne J. Hepburn, Graham J.C. Underwood
Department of Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 6 May 2009
Accepted 17 August 2009
Available online 26 August 2009

European intertidal salt marshes are important nursery sites for juvenile sh and crustaceans. Due to the
increasing threat of habitat loss, the seasonal changes of salt marsh sh communities need to be
understood in order to appreciate the ecological and economic importance of the saltmarsh habitat. This
study was the rst in Great Britain to investigate the seasonal changes of salt marsh sh communities
and the variation in community structure between closely located marsh habitats. Between February
2007 and March 2008, ve marshes on three estuaries of the Essex coastline were sampled using ume
nets to block off intertidal creeks at high tide. Fourteen sh species were caught. The community overall
was dominated by three species that made up 91.6% of the total catch: the common goby Pomatoschistus
microps (46.2% of the total catch), juvenile herring Clupea harengus (24.3%), and juvenile and larval sea
bass Dicentrarchus labrax (21.2%). Cluster analysis demonstrated clear seasonal patterns, with some
community structures unique to specic marshes or estuaries. The marsh sh community shifts from
a highly diverse community during spring, to a community dominated by D. labrax and P. microps in
autumn, and low diversity during winter months. Gravimetric stomach content analysis of sh
community identied three main trophic guilds; macroinvertivores, planktivores and omnivores. The
macroinvertivore feeding guild contained D. labrax and P. microps, the two most frequently occurring
species. This investigation demonstrates the importance of British salt marshes as nursery habitats for
commercial sh species.
2009 Elsevier Ltd. All rights reserved.

Keywords:
Great Britain
salt marshes
seasonality
sh
community composition
spatial variations

1. Introduction
Salt marshes are globally recognised as ecosystems that play an
important role in estuarine productivity and provide unique habitats for sh and invertebrates (Kneib, 1997). European salt marshes
are known to be important nursery sites for juvenile sh species
during high tide (Cattrijsse et al., 1994; Laffaille et al., 2000), when
sh move in from the surrounding mud ats and estuary channels
(Mathieson et al., 2000). Saltmarsh creeks in Europe are often
completely drained on the ebb tide, resulting in only a short period
of immersion for sh to move into the creeks and feed. Saltmarsh
creek sediments can harbour elevated densities of potential prey
compared to the adjacent sub-tidal area (Cattrijsse and Hampel,
2006). As a result, the energy expenditure of sh during inward
marsh movement is exceeded by the energy gained from feeding in
the marshes (Wolff et al., 1981). Ecologically, sh have an important
functional role in salt marshes, contributing to an outward ux of

* Corresponding author.
E-mail address: bcgree@essex.ac.uk (B.C. Green).
0272-7714/$ see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2009.08.008

particulate organic matter from the salt marsh (Laffaille et al., 1998;
Lefeuvre et al., 1999), whilst particular families such as the Muglidae accelerate benthic microalgal turnover through their feeding
methods (Laffaille et al., 2002).
Recently, it has been shown that sh communities in European
salt marshes alter in response to tidal, semi-diurnal and diel cycles
(Hampel et al., 2003), salinity gradients (Hampel et al., 2004), and
seasonal cycles (Cattrijsse et al., 1994; Laffaille et al., 2000), and that
sh feeding ecology is affected by these factors (Hampel et al.,
2005; Laffaille et al., 2001). The majority of research into sh
communities of European salt marshes has taken place along the
Schelde estuary, Belgium/Netherlands and Mont Saint-Michel Bay,
France. Salt marshes in Great Britain have received considerably
less attention (Frid, 1988; Kelley and Reay, 1988; Mathieson et al.,
2000). The seasonal changes of abundance, diversity and feeding
habits of salt marsh sh communities are yet to be addressed in
British marshes, and comparative studies between marshes elsewhere in Europe are few (Hampel et al., 2004, 2005; Koutsogiannopoulou and Wilson, 2007).
The coastline of the county of Essex contains 10.5% (4600 ha) of
the UKs remaining salt marshes (Environment Agency, 2004). This

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B.C. Green et al. / Estuarine, Coastal and Shelf Science 85 (2009) 247256

consists primarily of estuarine marshes along the rivers Stour,

Colne, Blackwater, Roach, Crouch and Thames, and coastal marshes
on the Dengie Peninsular and Hamford Water. Many of the Essex
estuaries are designated a Special Area of Conservation under the
EU Habitat Directive (number UK0013690), due to the large areas of
mudat, sandat and marsh present, and certain marshes (e.g.
Colne Point, Wrabness, see Fig. 1) are also individually protected as
Sites of Special Scientic Interest. The Essex estuaries harbour
juveniles of several commercially important sh stocks. Herring
larvae, Clupea harengus, are found in the Blackwater (Fox and
Aldridge, 2000) and Thames estuaries (Roel et al., 2004); the sea
bass, Dicentrarchus labrax, has spawning and nursery sites in the
Blackwater (Pickett et al., 2004); and the European eel Anguilla
anguilla is found in both the Colne, Blackwater (Bark et al., 2007)
and Stour (Rogers et al., 1998). Numerous species of sh larvae have
been sampled in the estuary plankton (Fox et al., 1999). Many
commercially important sh species are also caught as adults in the
estuary mouths (Rogers et al., 1998).
European salt marshes are at increasing risk from habitat loss.
The cause for habitat loss is not fully understood, although sea level
rise resulting in marsh loss through coastal squeeze is thought to be
a major factor (Van de Wal and Pye, 2004). Other studies theorise
that increased storm surges, increased Nereis diversicolor density in
marsh sediments and increased use of herbicides may all
contribute to habitat loss (Mason et al., 2003; Paramor and Hughes,
2004). The Essex coastline is no exception to this pattern of salt
marsh loss; the rate of marsh erosion on the river Blackwater from
1988 to 1997 was estimated to be up to 6 ha yr1 (Van de Wal and
Pye, 2004). With the increasing destruction of habitat through salt
marsh erosion and other anthropogenic inuences such as land
reclamation for agriculture and port construction, it is important to
investigate which sh species would be potentially affected if their
habitats and nursery sites were fragmented or lost.
As well as looking at taxonomic diversity, trophic diversity
through stomach content analysis and trophic guild construction
can assist in understanding the niche overlaps of species with
similar feeding requirements (Munoz and Ojeda, 1997). This can

present an alternative view of the assemblage through considering

ecological roles in the salt marsh environment. This technique can
be used to identify functional roles in the salt marsh ecosystem
(Mathieson et al., 2000).
Therefore, in this study we hypothesise that (a) seasonal
changes exist in the larval, juvenile and adult sh community that
inhabit the macrotidal salt marshes of the Essex coastline; (b) that
differences exist between sh communities of locally close marshes
over the seasonal cycle; and (c), that, through stomach contents
analysis, several trophic guilds can be found to exist in Essex salt
marsh sh communities.
2. Methodology
2.1. Study sites
Five salt marshes were sampled in this study. The marshes were
all located in the euhaline part of three estuaries, the Colne,
Blackwater and Stour, along the northern part of Essex coastline,
south-east England (Fig. 1). All the estuaries have a tidal range from
neap to spring tides of w1.54.5 m. Although the ve marshes were
spatially close, their size and geomorphologies were different
(Table 1). Plant surveys showed that the dominant stand on four of
the marshes was National Vegetation Classication (NVC) type
SM14a (Atriplex portulacoides dominated community), whilst
Abbots Hall marsh was SM14c (A. portulacoides with Puccinellia
maritima sub-community). All the marshes could be considered
well-established marshes (Long and Mason, 1983), with deep
(2.02.5 m) channels running through the marsh, of which shallower (1.01.5 m) creeks branch off. Only shallower creeks were
sampled in this study.
2.2. Sampling strategy and stomach content analysis
Marsh creeks were sampled using permanent ume nets,
adapted from designs by McIvor and Odum (1986) and Bretsch and
Allen (2006). The ume consisted of two walls of 2 mm

Fig. 1. The ve salt marshes sampled in this investigation (marked with diamonds) along the Essex coastline, south-east England. The local rivers and nearby large towns are also
marked.

B.C. Green et al. / Estuarine, Coastal and Shelf Science 85 (2009) 247256
Table 1
Geomorphological and oral properties of the ve salt marshes sampled during the
course of this study. Salt marsh area was measured using satellite imagery. The creek
area refers to the creeks used for sampling sh in this study. Two adjacent creeks
were sampled at Colne Point, creek a was used from 28th February to 18th May
2007, creek b was used from 11th June 2007 to 23rd January 2008. Salt marsh type
and drainage pattern was designated following Pye and French (1993), and identied through satellite imagery. Plant surveys were carried out following the National
Vegetation Classication; the type refers to the dominant stand on the salt marsh.
Marsh

Creek area
(m2)

Marsh type Drainage NVC

type

Colne
0.09
Blackwater 1.50

1514
(a) 1751 (b)
1033
440
1664

Stour

585

Embayment
Backbarrier
Fringing
Backbarrier
Fringing

Estuary

Area
(km2)

Abbots Hall Blackwater 0.39

Colne Point Colne
2.05
Pyeeet
Tollesbury
Fleet
Wrabness

0.07

Complex SM14c
Dendritic SM14a
Linear
SM14a
Complex SM14a
Reticulate SM14a

polypropylene mesh situated in the centre of the creek (Fig. 2). The
two walls were situated 1 m apart, with wings extending to the
bank of the creek, therefore funnelling nekton through the ume
on both the ood and ebb tides. The walls were supported by 8 cm
diameter wooden poles hammered into the sediment, situated
approximately 1.5 m apart.
During sampling, a 1.5  1.0 m weighted bag net, constructed of
the same mesh and supported by plastic bracing, was placed at the
seaward end of the ume, The mesh size for the bag net and ume
was 2 mm. Two wooden poles placed at the end of the ume kept
the net in position during sampling.
The mesh bag net was slotted in place at the end of the ume at
high tide, or once the water level had fallen parallel to the height of
the marsh surface. The net was kept in place during the ebb ow
and was removed once all the water had left the creek, therefore
sampling any nekton leaving the creek during the ebbing tide. A
small (25 cm) stream of water was left in the bottom of the creek
at low tide. When the bag net was retrieved, sh were counted and
identied on site. For each netting session, water samples were
taken at high tide, sampled at 0.5 m depth at the mouth of the creek
for salinity, dissolved oxygen and total suspended sediment (TSS).
Water temperature was also measured using a digital thermometer.
High tide dissolved oxygen water samples were measured in triplicate, using a modied method from Parsons et al. (1984).
One ume net was used per marsh. Flumes were located in
randomly selected marsh creeks, although creeks containing

249

sewage works run-off were avoided. We assumed that the umes

were neither attractants nor deterrents for nekton, and the selected
creeks were representative of the whole marsh. Abundance data
was standardised to number of sh 100 m2 of creek by dividing
the catch data for each species by the area of the creek upstream of
the net, measured using a GPS. Except for the Tollesbury Fleet site,
all the creeks used were cul-de-sac creeks and had no connection
to any other creek in the marsh (Table 1). The Tollesbury Fleet
marsh was composed of a maze of interconnecting creeks, and
creek area was estimated through monitoring water ow over
a tidal cycle, and assumed that sh followed the water ow when
exiting the marsh.
Creeks were sampled only when the high tide height was above
3.4 m (Harwich tide tables), the approximate height of mean high
water on the tidal curve. Sampling occurred from February 2007 to
March 2008, with the aim of sampling each site approximately once
per month. However, due to occasional mechanical failure of the
umes, this was not always possible. No sampling occurred during
July 2007.
As an alternative to taxonomic distribution, stomach content
analysis was used to assess sh functional distributions in terms of
trophic guilds. In the laboratory, the total length (TL) of all the sh
were measured to the nearest mm, and the wet weight to the
nearest 0.001 g. Stomach contents were assessed gravimetrically
(Hyslop, 1980). The contents were separated, identied to the
lowest taxonomic level possible and dried at 50  C until constant
weight. For every individual, the diet contents were expressed as
a gravimetric proportion (G%) (Hyslop, 1980), using G% (DW/
TW)  100, where DW is the dry weight of the individual prey item,
and TW is the total dry weight of the ingested food.
2.3. Data analysis
Once the catch data was standardised to sh 100 m2, the
community data was square root transformed to reduce the impact
of rare and highly abundant species. Due to the differing ecology of
the larval and adult/juvenile stages of Atherina presbyter and
Dicentrarchus labrax, these were taken to be separate species for
analysis purposes. Cluster analysis (complete linkage) using
PRIMER 6 software (Clarke and Gorley, 2006) was performed, and
clusters were interpreted at 21% similarity, the mean Bray-Curtis
similarity level for the complete dataset. SIMPER analysis was used
to determine species contributing the highest dissimilarity
between clusters, and ANOSIM was performed to identify signicant differences between clusters at 21% similarity. Sign tests were
used to check for differences in individual species abundance for
the whole year between different sampling sites. Sign tests were
used as seasonal data was not normally distributed, therefore the
individual species densities per site were compared to an overall
median for that species.
For analysis of stomach content data, average cluster analysis
(using complete linkage clustering) was performed to identify
trophic guilds. Clusters were interpreted at 40% similarity, the
mean Bray-Curtis similarity value for the whole dataset. ANOSIM
and SIMPER tests were performed to identify signicant differences
between diet composition of the trophic guilds and the food items
contributing to the dissimilarities between guilds.
3. Results
3.1. Environmental variables

Fig. 2. Schematic of ume net used to sample sh inhabiting salt marsh creeks. The
gure is not to scale. Wooden poles hammered into the sediment supported the net
walls. The net walls were 1.6 m high. The nets were permanent structures, and when
not in use the cod end bag net was removed to allow sh to move freely in and out of
the creek.

All four environmental variables measured across ve salt

marshes showed clear seasonal trends (Fig. 3). Temperature ranged
from 4  C in March and December 2007 to 23  C in June 2007. High

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B.C. Green et al. / Estuarine, Coastal and Shelf Science 85 (2009) 247256

Fig. 3. Seasonal changes in creek (a) water temperature, (b) salinity, (c) total suspended solids and (d) dissolved oxygen concentration of ve different salt marshes between
February 2007 and March 2008. Water samples were taken at 1 m depth in the mouth of the sampled salt marsh creek at exactly high tide. Dissolved oxygen data points are means
of three samples; total suspended sediment data points are means of two samples.

tide salinity was 3435 throughout the year apart from drops to
2530 during JanuaryFebruary due to high precipitation. Dissolved oxygen concentrations ranged from 1.7 ml l1 in June 2007
to 7.3 ml l1 in March and December 2007. Total suspended sediment (TTS) also showed a seasonal decrease from winter to
summer. Sign tests performed on the data showed that there was
no signicant difference in any environmental variables between
sites or estuary over the year, although the Colne estuary marshes,
Pyeeet and Colne Point, both showed consistently higher TSS
loads.

3.2. Species diversity and abundance

A total of 2821 individual sh belonging to 14 species were
caught in 45 sampling sessions between Feb 2007 and March 2008.
Of the 14 sh species caught, 87% were larvae or juveniles, and only
ve were present as adults (the sand smelt A. presbyter, 3-spined
stickleback Gasterosteus aculeatus, sand goby P. minutus, common
goby Pomatoschistus microps and snake pipesh E. aequoreus), 12
species had larvae present as a short seasonal peaks, with some rare
species occurring with less than 10 larvae caught over the whole
year (the garsh Belone belone, greater sand eel A. tobianus and
plaice P. esus). Abundance and species richness were both low in
the winter months. Total sh abundance at all sites (Fig. 4a)
remained low (below 5 sh 100 m2) between December and May,
but was almost always above 10 sh 100 m2 between May and
November. Species richness (Fig. 4b) increased during spring. The
highest number of sh species caught in one sample was during
MayJune 2008, with seven species being caught at Tollesbury
Fleet, Abbots Hall and Colne Point. During AugustDecember
species richness remained steady at approximately 4 species
sample1, but fell to between 0 and 2 species sample1 in February
and March of both years. The samples with the highest species

Fig. 4. Seasonal changes in (a) total abundance and (b) species richness of ve salt
marsh sh communities along the Essex coastline between February 2007 and March
2008. Each symbol represents an individual sample. No sampling took place during
July 2008.

B.C. Green et al. / Estuarine, Coastal and Shelf Science 85 (2009) 247256

richness did not correspond with to those with the highest abundance; the sample with the highest abundance (30/10/2007 at
Wrabness with an abundance of 59.4 sh 100 m2) was dominated
by two species (P. microps and Dicentrarchus labrax).
Five species contributed to 96.5% of the total sh abundance
(Fig. 4). The common goby Pomatoschistus microps was the most
numerous species caught over the year, with 1302 individuals
sampled (total length range 2249 mm). The herring Clupea harengus was second numerous with 684 individuals (total length range
3878 mm). There was one 3-day peak of C. harengus during 16th
18th May 2007 (at Pyeeet, Abbots Hall and Colne Point), during
which 628 of the total C. harengus sample were caught (with the
second highest abundance of 31.3 sh 100 m2). The sea bass
Dicentrarchus labrax was the third most abundant species, with
225 1 year juveniles (total length range 24108 mm) and 374 0
year larvae caught. Juveniles were present from April 2007 to
February 2008 whilst larvae were only present MayOctober 2007.
Juvenile sprat, Sprattus sprattus (total length range 5988 mm), had
77 individuals caught during the year, although 90% of these were
caught in JanuaryFebruary 2008. The nal dominant species was
the sand smelt, A. presbyter, where 61 juveniles and adults (total
length range 39119 mm) were caught between March and October
2007. The remaining 3.5% of the total abundance was contributed
by 9 species, 5 of which were only caught between April and June
2007 (A. tobianus, B. belone, E. aequoreus, P. minutus, P. platessa)
(Fig. 5).
Non-parametric sign tests were used to identify signicant
differences between sites in abundance of individual species over
the course of the 13 months sampling. Wrabness salt marsh
showed signicantly higher densities of Pomatoschistus microps
compared to all other sites, while both of the Blackwater estuary
sites showed signicantly lower densities of juvenile Dicentrarchus
labrax than all other sites (Abbots Hall P < 0.01; Tollesbury Fleet
P < 0.05).
Many invertebrates were also caught during sampling; the
ctenophore Pleurobrachia pileus, shrimps Palaemon longirostis and
Crangon crangon and the shore crab Carcinus maenas were caught at
all sites between March and November. The scyphozoans Aurelia
aurita, Cyanea capillata and C. lamarckii were caught at Abbots Hall
and Tollesbury Fleet between May and June 2007.

251

3.3. Cluster analysis

The cluster analysis (complete linkage) of the samples identied
ten clusters at the 21% similarity slice (the mean Bray-Curtis similarity value for the whole data set) on the basis of community
structure (Fig. 6). The clusters were all signicantly different in
community structure (ANOSIM global R 0.923, p < 0.001), apart
from two dates, which were merged into the proximal cluster.
SIMPER analysis was used to identify which species contributed to
the highest dissimilarity between clusters (Table 2).
The clusters reveal a sh community with complex seasonal
dynamics. The clusters can be grouped into three temporal sets.
Clusters A, B, C, D and E represent the period between April and
June 2007 (Table 2), characterised by high diversity due to the
presence of a spring peak of sh larvae, with species present that
had less than 10 individuals sampled over the year (e.g. juvenile
sand eel Ammodytes tobianus and larval garsh Belone belone).
Particularly, cluster D shows a spring peak of Clupea harengus
larvae, which corresponded with a temporary drop in other species
such as Pomatoschistus microps abundance (mean of 0.10  0.01 sh
100 m2) compared to other samples taken at the same time of
year. These larval uxes were sometimes spatially restricted, with
the C. harengus larvae ux only being observed in the sites on the
Colne and Blackwater estuaries, while D. labrax larvae were only
observed in high densities in sites on the Colne estuary (cluster E).
Clusters F and G represent the period between September
December during which diversity in the salt marsh sh community
was reduced and only Pomatoschistus microps and juvenile Dicentrarchus labrax were the commonly recorded species (Table 2). The
clusters differ by the lower densities of P. microps and D. labrax in
cluster F than G. The very high population of P. microps in cluster G
was due to the large number of juvenile recruits observed in the salt
marshes (mean of 18.80  9.8 sh 100 m2). The two clusters,
although covering sampling dates over the same months, do show
some spatial differences; cluster G predominantly contains salt
marshes from Colne Point and Wrabness, while cluster F is
composed mostly of salt marshes from the Blackwater estuary.
Clusters H, I, and X and part of cluster F are all from the winter
period of DecemberMarch (Table 2), with Cluster X being samples
when no sh were caught. The clusters are dened by lower

Fig. 5. Seasonal changes in sh species abundance in Essex salt marsh creeks between February 2007 and March 2008 (separated by life stages for A. presbyter and D. labrax)
sampled across ve salt marshes on three estuaries. No sampling took place during July. Upward pointing ticks on the x-axis represent individual sampling dates.

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B.C. Green et al. / Estuarine, Coastal and Shelf Science 85 (2009) 247256

Fig. 6. Cluster analysis (Bray-Curtis similarity, complete linkage) of square root transformed CPUE of species recorded in ve salt marshes between February 2007 and March 2008.
The slice is at a similarity of 21%, with clusters termed X being samples with a total CPUE of zero, and therefore 0% similar to any other sample. The ten clusters all show
signicantly different communities from other clusters. The clusters are lettered in an approximate temporal sequence. The dates of 11/02/2007 and 21/02/2008 were merged into
clusters D and A respectively as they showed no signicant difference to any other cluster.

diversity, lower Pomatoschistus microps and D. labrax abundance

and the presence two species predominantly abundant during
winter; the sprat S. sprattus and the pipesh S. typhle. The clusters
show no denition by site or estuary.
3.4. Stomach content analysis
Stomach content analysis of 216 individual sh (from 10 of the
16 species caught) identied 15 different categories of food
ingested across, plus one category of unidentied matter. The
three most frequently occurring food categories were copepods
(42% of samples), polychaetes (28%) and unidentied matter (28%)
(Table 3). Discounting species with less than two individuals
sampled, S. sprattus had the most diverse diet, with an average of

1.81 different food types sample1, followed by Dicentrarchus labrax (1.64 food types sample1) and A. presbyter (1.37 food types
sample1). Dicentrarchus labrax was the only species that showed
a seasonal difference in its diet, with no amphipods found in its
stomach during spring months (AprilJune), and a mean amphipod
content of 29.58  5.2% in Autumn and Winter months (August
February).
Analysis of the species diet proportions showed there were three
trophic guilds present in the salt marshes (designated as macroinvertebrate feeders, plankton feeders and omnivorous feeders)
when a similarity slice is taken at 36 %, the mean Bray-Curtis similarity level for the dataset (Fig. 7). An ANOSIM test performed on the
groupings showed the majority of clusters to be signicantly
different from one another (global R 0.127, P < 0.001). SIMPER

Table 2
Properties of individual clusters from the dendrogram in Fig. S1, from sh community sampling in ve salt marshes between February 2007 and March 2008. N refers to the
number of samples in each cluster, and the corresponding month and sampling site in the Dates and Sites row respectively (salt marsh abbreviations: AB Abbots Hall, CO
Colne Point, PY Pyeeet, TO Tollesbury Fleet, WR Wrabness). Mean species n refers to the mean species richness for each cluster  S.E. The sh species that contributes to
the highest dissimilarity between other clusters is termed the Dening Species, with its mean Dening Abundance for that cluster expressed as sh 100 m2.
Cluster (N)

A (4)

B (3)

C (2)

D (5)

Dates
Sites
Mean Species n
Dening Species
Dening Abundance

February and April

CO, PY
3.3  0.9
A. minuta
0.44  0.1

March, May, June

AB, CO, TO
4.0  1.0
P. microps
0.01  0.0

April, June
AB, WR
5.0  2.0
P. microps
1.20  0.4

May
AB, CO, PY, TO
4.4  1.7
C. harengus
9.96  5.7

Cluster (N)

E (5)

F (11)

G (7)

H (2)

Dates
Sites
Mean Species n
Dening Species
Dening Abundance

June, August
CO, PY
3.4  0.6
D. labrax larvae
11.12  4.2

September-December
AB, PY, TO, WR
2.2  0.4
P. microps
2.05  0.4

September-November
CO, WR, PY
3.4  0.3
P. microps
18.8  6.4

January
CO, PY
4.0  1.0
S. sprattus
3.4  2.5

Cluster (N)

I (2)

X (4)

Dates
Sites
Mean Species n
Dening Species
Dening Abundance

December, February
AB, CO
1.5  0.5
D. labrax juveniles
0.12  0.1

March
AB, CO, PY, TO
0.0  0.0

Table 3
Gut content analysis and the mean gravimetric proportion (G%) of dry weight diet content (standard error) of 11 salt marsh-utilizing sh species, summed for season and site. Fullness index was calculated with sh dry weight
estimated at 80% of wet weight. Samples were taken between February 2007 and March 2008 from ve salt marshes along the Essex coastline. Unidentied material consists of liqueed stomach contents, plus other unidentied
food fragments.
B. belone

C. harengus

S. sprattus

G. aculeatus

P. microps

D. labrax (juvenile)

D. labrax (larvae)

C. labrosus

E. aequoreus

49
3.88  0.31
80.92  1.66
0.67  0.10

1
0.07
31.00
0.56

12
0.62  0.15
48.08  2.96
0.94  0.15

11
2.30  0.29
74.36  3.41
0.22  0.05

50
0.58  0.04
38.40  0.71
0.92  0.17

65
3.34  0.41
61.08  2.09
1.17  0.11

0.89  0.29
50.00  2.31
0.22  0.05

14
0.40  0.03
37.13  1.12
1.28  0.14

2
215.50  32.50
-

Mean G% ( S.E.)
Diatoms
Macroalgae

0.00  0.00
2.26  2.05

0.00
0.00

0.00  0.00
0.00  0.00

0.00  0.00
2.11  2.11

0.00  0.00
0.00  0.00

0.00  0.00
17.61  5.32

0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00

33.30  12.60
0.00  0.00

0.00  0.00
0.00  0.00

Nematodes

0.00  0.00

0.00

0.00  0.00

0.00  0.00

0.00  0.00

0.00  0.00

0.20  0.20

0.00  0.00

0.00  0.00

0.00  0.00

Polychaetes

4.51  1.93

0.00

8.33  8.33

7.68  5.15

16.70  16.70

35.10  6.52

25.12  4.95

0.00  0.00

0.17  0.17

0.00  0.00

Gastropods
Bivalves

2.29  1.70
0.15  0.15

0.00
0.00

0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00

46.32  6.92
0.01  0.01
0.05  0.05
3.56  2.41
0.00  0.00
1.28  1.28
0.00  0.00

100.00
0.00
0.00
0.00
0.00
0.00
0.00

80.90  11.10
0.00  0.00
0.00  0.00
0.13  0.13
0.00  0.00
0.00  0.00
0.00  0.00

64.70  13.40
0.00  0.00
0.00  0.00
2.06  2.06
0.00  0.00
0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00

37.12  6.74
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00
0.02  0.00
0.00  0.00

19.53  4.74
0.00  0.00
0.00  0.00
26.60  4.76
0.17  0.17
4.63  2.37
5.04  2.40

98.00  2.00
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00

13.52  9.07
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00
0.00  0.00

0.00  0.00
0.00  0.00
0.00  0.00
1.02  1.02
0.00  0.00
0.00  0.00
0.00  0.00

Insects

0.00  0.00

0.00

2.45  2.08

13.53  8.97

33.30  33.30

0.22  0.22

2.29  1.51

0.00  0.00

26.30  11.70

49.00  49.00

Teleosts

0.00  0.00

0.00

0.00  0.00

0.00  0.00

0.00  0.00

0.06  0.06

0.00  0.00

0.00  0.00

0.00  0.00

36.29  6.40

0.00

8.07  8.07

9.95  9.05

50.00  28.90

9.81  3.92

16.38  3.96

2.00  2.00

26.50  11.70

Copepods
Ostracods
Cumaceans
Amphipods
Isopods
Decapods Caridea
Decapods Brachyura

Unidentied Material

0.03  0.01
17.80  1.46
2.32  0.67

B.C. Green et al. / Estuarine, Coastal and Shelf Science 85 (2009) 247256

A. presbyter (adult)
Species Parameters ( S.E.)
Number of individuals examined
Mean Wet Weight (g)
Mean Length (mm)
Mean Fullness Index

0.00  0.00
50.00 50.00

253

254

B.C. Green et al. / Estuarine, Coastal and Shelf Science 85 (2009) 247256

Fig. 7. MDS plot of Bray-Curtis similarities between average compositions of dry

weight stomach contents (measured gravimetrically) of 11 sh species caught in 5 salt
marshes between February 2007 and March 2008. The four types of symbols represent
signicantly different groupings at 39% similarity, with SIMPER analysis used to
designate the groupings as different trophic guilds. The text above each symbol
represents the rst letter of the genus name and rst three letters of the species name,
except Dlal, representing D. labrax larvae. See Fig. 4 for the list of species caught.
Symbols with asterisks indicate the 6 species (D. labrax juveniles and larvae summed
together) whose total abundance contributes to 96.5% of the total abundance of sh
caught in this study.

analysis showed that the macroinvertebrate feeders consist of

juvenile D. labrax and Pomatoschistus microps, whose diet consists of
primarily of polychaetes (mean G% 30.1%) and copepods (28.3%).
The planktonic feeders diet consisted almost entirely of copepods
(78.0%), although a mixture of benthic invertebrates were also
present (8.4%) whilst omnivorous feeders show a mixture of
unidentiable material (42.4%), insect remains (27.2%), diatoms
(11.1%) and polychaetes (5.6%).
4. Discussion
4.1. Seasonal changes in the salt marsh sh community
To the best of our knowledge, this study is the rst to analyse the
seasonal changes of sh communities in salt marshes in Great
Britain. The study has demonstrated clear changes in sh communities over one year and also shown signicant differences in
community structure between closely located salt marshes. The sh
communities of the salt marshes of the Essex coastline resemble
those found in other salt marshes around the English Channel and
North Sea with the dominance of Dicentrarchus labrax and Pomatoschistus microps (Cattrijsse et al., 1994; Frid, 1988). However, other
sites in north-west Europe have other species dominating the sh
community, such as mullet Liza ramada in Mont Saint Michel Bay,
France (Laffaille et al., 2000), or stickleback G. aculeatus in Dublin
Bay, Ireland (Koutsogiannopoulou and Wilson, 2007). A high
proportion of the species (50%) caught in this study could be
considered economically important, which is comparable with
64.7% from Castro Marim marsh, Spain, (Veiga et al., 2006) and 60%
from Dublin Bay, Ireland (Koutsogiannopoulou and Wilson, 2007),
reiterating the importance of European salt marshes as nursery
habitats for commercial sh, and the need for increased conservation of the saltmarsh habitat. However, only the common goby
P. microps and the sea bass D. labrax had an almost constant presence
in the marsh throughout the year. This supports the theory of Cattrijsse et al. (1994), based on a study of marshes along the Schelde
estuary that D. labrax and P. microps could be considered the only

two sh species in north west Europe to fully utilise salt marshes as

nursery sites throughout the year and throughout their entire larval
and juvenile stages. Our data showed high levels of patchiness
within short temporal periods for individual species abundances,
especially with P. microps (Fig. 4). Cattrijsse et al. (1994) suggested
that patchiness in P. microps may be inferred through close association with water temperature. However, the ne-scale distribution
of the dominant sh species caught did not correlate with the other
environmental variables measured in this study (Fig. 2). Other
unmeasured factors may be the cause of a proportion of the patchiness observed in this study; light intensity is known to inuence bay
anchovy (Anchoa mitchilli) inhabiting marsh creeks in the USA (Reis
and Dean, 1981), whilst foraging activity of P. microps changes with
semi-lunar cycles (Hampel and Cattrijsse, 2004), and this could
inuence their extent of migration in marsh creeks.
The most numerous sh sampled was the common goby
Pomatoschistus microps. Pomatoschistus is commonly the most
abundant genus in European salt marsh sh communities, whether
dominant as P. microps (Cattrijsse et al., 1994; Veiga et al., 2006),
P. minutus or P. lozanoi (Frid, 1988; Laffaille et al., 2000). The
seasonal distribution of P. microps in the Essex marshes (Fig. 5)
matches that of Koutsogiannopoulou and Wilson (2007) in Dublin
Bay, Ireland. The species benets from both high salinity and
temperature tolerances (Dolbeth et al., 2007), allowing it to inhabit
marshes over the entire estuarine range and shelter in the marsh
pools, even in the heat of summer (Hampel et al., 2004). Pomatoschistus microps spawns from March to June (Pampoulie et al.,
2000), hence the population peak in the Autumn months was due
to newly recruited juveniles being present (Fig. 5).
However, not all the sh species found in the Blackwater, Colne
and Stour estuaries utilise the salt marshes. As well as the species
observed in this study, sole (Solea solea), cod (Gadus morhua),
whiting (Merlangius merlangus), ray (Raja sp.) and pogge (Agonus
cataphractus) are all caught by commercial shermen within the
three estuaries (Pawson et al., 2002; M. Hardy, pers comm.), none of
which were present as adults or juveniles in the salt marshes.
The design of the ume net in this study aimed to be as efcient
as possible when sampling sh. Recovery efciency estimates for
similarly designed gear was 8394% (Bretsch and Allen, 2006) and
73% (McIvor and Odum, 1986) for Fundulus heteroclitus, the North
American functional equivalent of Pomatoschistus microps (Cattrijsse et al., 1994), therefore it cannot be assumed that our ume
nets were 100% efcient. However, the gear used was the best
option with the least disadvantages for sampling the salt marsh
habitat, compared to other methods such as trapping, fyke nets and
drop nets (Rozas and Minello, 1997).
The sampling strategy of this study meant that samples were
taken across a restricted range of high tide heights. To minimize any
semi-lunar inuences on the data, we sampled the salt marsh
creeks from the mean high tide height (3.4 m chart datum at Harwich) and the spring tides above this height. The lowest high tide
height at Harwich is 2.8 m, and during these neap tides some marsh
creeks are inaccessible to sh. Although species such as Pomatoschistus microps occur at lower densities in salt marsh creeks during
neap tides (Hampel et al., 2003), we believe the range of high tide
heights sampled resulted in minimal semi-lunar inuence over the
community structure.
4.2. Trophic structure and the sh community
The numbers of sh species that utilise salt marshes vary around
Europe. Laffaille et al. (2000) observed 31 species over three years in
Mont Saint Michel Bay, France, while Koutsogiannopoulou and
Wilson (2007) observed only 10 over two years in Dublin Bay.
However, in this investigation, only two species of the 14 caught,

B.C. Green et al. / Estuarine, Coastal and Shelf Science 85 (2009) 247256

255

Pomatoschistus microps and juvenile (1) D. labrax, both part of the

macroinvertivore feeding guild (Fig. 7) were present almost
throughout the entire year. The omnivorous feeding guild was the
least abundant guild due to it containing sh (C. labrosus, E. aequoreus,
G. aculeatus) that were relatively scarce in the marshes.
The comparative abundances of the trophic guilds could be
a result of the seasonality of their diet. The zooplankton that
composes the predominant part of the diet of planktivores such as
Clupea harengus and A. presbyer (Table 3) is often subjected to
seasonal patterns in estuaries; Tackx et al. (2005) observed variations of 10  103 mesozooplankton m3 in winter to 267  103
mesozooplankton m3 in August in the Zeeschelde estuary. Similar
patterns were observed in the Westerschelde by Soetaert and Van
Rijswijk (1993). However, although some infaunal food items such
as amphipods have seasonal patterns of abundance in salt marshes
(Cattrijsse et al., 1994), polychaetes such as Nereis sp., Nephtys sp.
and oligochaetes have limited seasonal changes in abundance in
the nearby Norfolk salt marshes (Frid and James, 1989), so benthic
food items may not limit the abundance of sh feeders at any time
during the year. As well as seasonal changes, the substantial
biomass of prey items available in the salt marsh suggests that
benthic infauna cannot be limiting. The highest minimum
consumption of available benthic prey items by D. labrax and
Pleuronectes platessa was estimated at 0.035% of the population of
prey for the whole year in Schelde marshes (Hampel et al., 2005).
This means that there was effectively an inexhaustible supply of
food available all year round, which can be constantly utilised by
benthic feeding sh. Conversely, winter zooplankton densities
could have been low enough to the extent where feeding in the
estuary and salt marsh becomes inefcient, and to feed offshore
would be more advantageous for planktivorous sh. Omnivorous
species, such as the mullet C. labrosus also show distinct seasonal
patterns in abundance, however their primary food source, benthic
diatoms, do not show a strong seasonal abundance in the Colne
estuary (Thornton et al., 2002).
In this study, sh were only sampled for stomach contents on
the ebb tide; therefore it is a possibility that a shs prey was
consumed elsewhere before being caught in the salt marsh creek.
However, Laffaille et al. (2001) demonstrated that 0-year D. labrax
caught on the ebb have a signicantly higher feeding index
(stomachs that contain food) than those caught on the ood tide in
salt marsh creeks. Although it is not known whether this reasoning
can be applied to all sh species sampled in this study, we have
assumed that all species follow a similar pattern to that identied
by Laffaille et al. (2001). This is supported by the fullness index of D.
labrax in this study (mean of 1.17) is similar to that found by Hampel
et al. (2005) (ranging from 0.69 to 2.13).

harengus was only observed in marshes on the Blackwater and

Colne estuaries, as the herring spawning site, Eagle Bank, is in the
mouth of the Blackwater (Fox and Aldridge, 2000). Conversely,
although D. labrax has nursery and spawning sites in the Blackwater (Pickett et al., 2004), it was highly abundant in all three
estuaries sampled in this study.
Certain clusters (Table 2) contained samples collected over
a short period from two marshes that were from separate estuaries
(e.g. cluster G, from Wrabness and Colne Point). This demonstrates
that although the ve marshes sampled were identical in salinity,
plant communities and other environmental variables measured
(Fig. 3), and that food abundance may be a key driver over seasonal
distributions, there are other factors that dominate sh community
structure between salt marshes.
Other factors that could be responsible for the variation in
community structure and species abundance include the landscape and spatial characteristics of the individual salt marshes.
Allen et al. (2007) identied species preferences for particular
geomorphological features of North American salt marsh creeks,
although no single feature determined total abundance. Spatial
features such as marsh area and nearest neighbour may have an
impact on community structure as shown with seagrass beds
(Bostrom et al., 2006; Connolly and Hindell, 2006). However,
though the area of marshes sampled in this study ranged from
0.09 to 2.05 km2 (Table 1), no signicant differences between sh
assemblages related to marsh size were observed in the cluster
analysis (Table 2), although other spatial features may impact on
the sh community. The overall intertidal landscape may also alter
community structure through habitat connectivity and inuences
of adjacent ecosystems such as intertidal mud and sand ats,
which is known to inuence sh in North American salt marshes
(Irlandi and Crawford, 1997). These inuences on the sh
community remain unexplained in the saltmarsh landscape.

4.3. Inter-marsh differences

Allen, D.M., Haertel-Borer, S.S., Milan, B.J., Bushek, D., Dame, R.F., 2007. Geomorphological determinants of nekton use of intertidal salt marsh creeks. Marine
Ecology Progress Series 329, 5771.
Bark, A., Williams, B., Knights, B., 2007. Current status and temporal trends in stocks
of European eel in England and Wales. ICES Journal of Marine Science 64,
13681378.
Bostrom, C., Jackson, E.L., Simenstad, C.A., 2006. Seagrass landscapes and their
effects on associated fauna: a review. Estuarine Coastal and Shelf Science 68,
383403.
Bretsch, K., Allen, D.M., 2006. Tidal migrations of nekton in salt marsh intertidal
creeks. Estuaries 29, 464468.
Cattrijsse, A., Hampel, H., 2006. European intertidal marshes: a review of their
habitat functioning and value for aquatic organisms. Marine Ecology Progress
Series 324, 293307.
Cattrijsse, A., Makwaia, E.S., Dankwa, H.R., Hamerlynck, O., Hemminga, M.A., 1994.
Nekton communities of an intertidal creek of a European estuarine brackish
marsh. Marine Ecology Progress Series 109, 195208.
Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, p. 190.
Connolly, R.M., Hindell, J.S., 2006. Review of nekton processes and ecological
processes in seagrass landscapes. Estuarine, Coastal and Shelf Science 68,
433444.

This study is one of few that have studied more than one salt
marsh over a particular time period (Hampel et al., 2004, 2005).
Sampling simultaneously ve salt marshes on three estuaries
within 50 km of each other highlights the inter-marsh variability in
assemblage structure, even between marshes on the same estuary
(Table 2). A key area of other studies was the focus on temporal
rather than spatial patterns, and the variability of sh communities
between marshes would not have been observed (Koutsogiannopoulou and Wilson, 2007; Veiga et al., 2006). This study has shown
that marshes do vary over a small geographical area, and that
replicate marshes cannot be assumed to be equally important for
conservation status or ecological function.
Large seasonal changes in abundance of some species (A. presbyter, P. microps, juvenile D. labrax) were found at all sites. Other
species were more restricted; the sudden spring inux of Clupea

Acknowledgements
This research was supported by a PhD studentship awarded to
BG by the Natural Environment Research Council (Award Code
NER/S/A/2006/14133). BG would like to thank his many sampling
assistants, especially Mr Jason Argent, Mr John Green, Mr Russell
Smart and Miss Emma Thorpe. The authors are grateful to the Essex
Wildlife Trust and Mr Simon Garnham for permission to sample on
their marshes.

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