Download LITERATURE STUDY: SHOREBIRDS AND THEIR ABIOTIC

LITERATURE STUDY:
SHOREBIRDS AND THEIR ABIOTIC
ENVIRONMENT
Relation between Shoal Morphology and Shorebirds in the
Westerschelde Estuary
Vanermen, N.
De Meulenaer, B.
Stienen, E.W.M.
Research Institute for Nature and Forest
Ministry of the Flemish Government
Kliniekstraat 25
B-1070 Brussels
Report INBO.A.169
November 2006
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INTRODUCTION.............................................................................................................................. 1
SHOREBIRD DISTRIBUTION: PREDICTING VARIABLES ............................................................ 3
2.1 Benthos ...................................................................................................................................... 3
2.2 Sediment .................................................................................................................................... 4
2.3 Emersion time............................................................................................................................. 5
2.3.1
Low tide counting bias ....................................................................................................... 5
2.3.2
Emersion time as a predictor in bird distribution................................................................ 6
2.4 Drainage channels...................................................................................................................... 7
2.5 Salinity ........................................................................................................................................ 7
2.6 Distance to high water roosts ..................................................................................................... 8
2.7 Predators .................................................................................................................................... 8
2.8 Prey availability........................................................................................................................... 9
2.9 Shoal morphology..................................................................................................................... 10
3 SPECIES: HABITAT DEMANDS ................................................................................................... 13
3.1 Oystercatcher (Haematopus ostralegus).................................................................................. 13
3.2 Avocet (Recurvirostra avosetta) ............................................................................................... 15
3.3 Ringed plover (Charadrius hiaticula) ........................................................................................ 17
3.4 Kentish plover (Charadrius alexandrinus) ................................................................................ 19
3.5 Grey plover (Pluvialis squatarola) ............................................................................................ 21
3.6 Knot (Calidris canutus) ............................................................................................................. 23
3.7 Sanderling (Calidris alba) ......................................................................................................... 25
3.8 Dunlin (Calidris alpina) ............................................................................................................. 27
3.9 Bar-tailed godwit (Limosa lapponica) ....................................................................................... 29
3.10
Curlew (Numenius arquata) ................................................................................................. 31
3.11
Spotted redshank (Tringa erythropus) ................................................................................. 33
3.12
Redshank (Tringa totanus)................................................................................................... 35
3.13
Turnstone (Arenaria interpres)............................................................................................. 37
4 EXPERT INQUIRY ......................................................................................................................... 39
4.1 Introduction............................................................................................................................... 39
4.2 Sediment .................................................................................................................................. 39
4.3 Emersion time........................................................................................................................... 41
4.4 Food choice .............................................................................................................................. 42
1 INTRODUCTION
To improve the accessibility of the economically important port of Antwerp, a widening of the shipping
channel is being planned. However, the Westerschelde has large ecological significance as well, and
the area is therefore protected under the Birds and Habitat Directive (VHR) and the Water Framework
Directive (KRW). These European Directives have made requirements in terms of substantiation,
effect forecasting, mitigation or compensation during the planning stages of system alterations more
strict. The project ZEEKENNIS aimed at ensuring appropriate responses to future area management
issues, and both available water system expertise and forecasting method accuracy have been
upgraded. The final report of the project ZEEKENNIS describes the expertise developed in the five
foregoing years and now there exists better insight in the working of the Westerschelde ecosystem,
which will allow better analysis and forecasting of alteration-effect relations. Yet questions concerning
area management and policy remain, which cannot be answered completely in the absence of certain
elements of expertise and insight or methods (Kater, 2005).
In project plan LTV O&M of December 12th 2005, under Objective 2 – estuary restoration – the
following problem was formulated: “To achieve the aims as stated in Streefbeeld (Target definition)
2030 VHR and KRW, simply being able to determine the impact of human intervention in the
Westerschelde ecosystem (e.g. broadening of the waterway) on the habitat acreage will not be
sufficient; it will also be necessary to determine which habitat factors are of real importance to the
various organisms. To this end, reliable information and insight must be made available regarding the
relationship between physical, biological and chemical processes and the habitats on the one hand,
and the relationship between the habitats and the organisms on the other. At present this information
is largely unavailable.”
The relevant policy and management questions are therefore: what are the ecological effects resulting
from physical changes in the Westerschelde estuary caused by human or other interventions?
In the project plan, two research issues have been identified:
•
•
Which habitat factors are of true importance; where and how much of each type of habitat is
desirable and what is the response of the acreage and its users (e.g. water birds) to certain
interventions?
How can the effects of changes in turbidity on primary production and higher trophic levels be
charted?
One activity geared to answer these questions is an investigation into the relationship between shoal
morphology and waders. The first step in any such an investigation is to acquire an overview of
worldwide available knowledge with regard to the relationship between waders and shoal morphology
(comparable with the situation in the estuary of the Westerschelde). The investigation is to restrict
itself to those shorebird species designated in Natura 2000 (European Bird guidelines). Shorebirds
named in this guideline are as follows: oystercatcher (Haematopus ostralegus), avocet (Recurvirostra
avosetta), ringed plover (Charadrius hiaticula), Kentish plover (Charadrius alexandrinus), grey plover
(Pluvialis squatarola), knot (Calidris canutus), sanderling (Calidris alba), dunlin (Calidris alpina), bartailed godwit (Limosa lapponica), curlew (Numenius arquata), spotted redshank (Tringa erythropus),
redshank (Tringa totanus) and turnstone (Arenaria interpres).
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2 SHOREBIRD DISTRIBUTION: PREDICTING VARIABLES
In this chapter an overview is given of the variables influencing shorebird distribution. These include
biotic as well as abiotic variables. It is discussed which of the mentioned parameters might be affected
by a future channel widening. The density of benthic prey has to be sufficiently high to meet the daily
energy requirements of staging shorebirds. However, prey densities alone are insufficient to predict
shorebird densities since availability of the prey may be equally important. Availability of benthic prey
is affected by several abiotic and biotic factors, such as tidal stage, sediment characteristics,
morphology of the intertidal flat, exposure period or distance to high water roosts. Apart from benthos
some other biotic factors play a major role in wader distribution too, such as the shorebird density
itself, or the risk of being predated by birds of prey.
2.1 Benthos
As a rule, there is a positive correlation between densities of shorebirds and their prey as found by,
for example, Goss-Custard (1970), Zwarts (1981), Esselink (1982), Roukema (1984), Meire (1993),
Kalejta & Hockey (1993) and Yates et al. (1993). However, the strength of these relations varies
among studies, and studies conducted at fine spatial scales often result in weak correlations. Yates et
al. (2003) quote that strong correlations between prey density and shorebird abundance is most
obvious when their diet is well known and that predictability increases with increasing diet
specialisation of the concerned shorebird species. According to Kalejta & Hockey (1993), densities of
visual foragers like grey plovers are predicted better by using prey biomass rather than by using prey
densities. Visually foraging waders seem to be able to assess prey size and profitability prior to
handling the prey (Kelsey & Hassal, 1989; Kalejta & Hockey, 1993). Thompson (1986) and Colwell &
Landrum (1993) also state that prey density alone is insufficient to account for the distribution of birds
because often, the mean size of individual prey items at high densities is smaller and prey is thus less
profitable than at intermediate densities.
It is in fact not easy to link shorebird distribution with prey densities. The shorebird’s diet consists of
more than one species and the total food availability can not be determined by simply adding the total
flesh mass of all these species. Individual birds decide where to forage based on their expected food
intake rate rather than based on food density. As reviewed by Goss-Custard (1985), many studies
show that attractiveness of an area to shorebirds largely depends on the rate at which they can feed
there. The food intake depends on several factors like prey density, prey size, calorific content,
digestibility, burying depth and surface activity, which all partly determine the harvestable food
availability (e.g. Zwarts & Blomert, 1992; Zwarts et al., 1992). Furthermore, intake rate is influenced by
interference between foraging birds, and hence depends on the bird density itself. Interference results
from prey depletion, disturbance, restriction of the field view and kleptoparasitic pressure.
As already mentioned and as summarized in Figure 1, only a small fraction of the total prey population
is harvestable to a specific shorebird species. Five requirements have to be taken into account. First
of all, the prey must be accessible; some for example live out of reach of the bill of the bird, or are
protected by a hard shell. There is evidence that the bill length exactly determines which prey is
accessible and which is not (Zwarts & Wanink, 1984; Zwarts et al., 1996). Secondly, the prey must be
detectable, and this primarily depends on prey activity (visual foragers) or sediment characteristics
(tactile foragers). Thirdly, the birds have to be able to swallow the prey. Knots for example are able to
swallow Baltic tellin (Macoma balthica) of 16mm long, but spit out any larger ones (Zwarts & Blomert,
1992). Furthermore, the prey must be digestible. Wader species that swallow shellfish whole (e.g. the
knot) need to spend energy crushing it in their stomach. Other shorebirds open their prey to extract
the well digestible flesh (e.g. the oystercatcher), however, they need longer handling times. Last of all,
prey must be profitable. Some prey is refused because their handling efficiency (intake per unit of time
handling the prey) is too small. In general, handling efficiency increases with increasing prey size, and
prey that is too small can be ignored. For example, knots ignore clams (Mya arenaria) that are smaller
than 4mm, and curlews only eat Mya arenaria that are longer than 25mm (Zwarts & Wanink, 1984).
This lower limit can be explained by the fact that handling efficiency is lower than intake rate in eating
this small prey.
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Total prey population
Accessible fraction
Burried too deep
Invisible
…
Not ingestable
Not gaping
Available fraction
Not profitable
Harvestable fraction
Figure 1. Different fractions of the total prey population and the fraction that is harvestable to the predator (after
Meire, 1993)
The densities of benthic invertebrates show a strong seasonal and year-to-year variation, which may
have major effects on shorebird foraging and activity patterns. Also spatial patterns in benthic prey can
vary in time and species composition may change rapidly (e.g. Puttick, 1984; Beukema et al.,1993;
Zwarts & Wanink, 1993).
Finally, a major practical problem in using food availability to predict shorebird densities or shorebird
distribution is that the quantification of invertebrate populations in large intertidal areas can only be
achieved at very high costs and is very time consuming (Ens et al., 2005; Stillman et al., 2005).
2.2 Sediment
There are several ways to describe sediment type, unfortunately these methods do not always give
comparable results. A measure often used in the Netherlands is the lutum-content. Lutum-particles are
defined as particles being smaller than 2 µm. Another frequently used measure is the median grain
size. In the Wadden Sea, there is a strong correlation between lutum content and the median grain
size, however, the exact nature of the relationship may differ between sites. Furthermore the amount
of organic matter, calcium, surface pooling, presence of ripples and the depth of the oxygenated soil
layer are all strongly correlated with the lutum-content. As the proportion of lutum increases, the waterholding capacity of the tidal flat also increases. Nowadays advanced techniques using laser-particle
sizers are increasingly used to characterise the sediment. However, direct comparison with more
classic methods is not possible because calibration studies have not yet been conducted (van de Kam
et al., 1999; Blomert, 2002).
There is a strong relationship between biomass of benthic animals and the sediment type. For
example cockles (Cerastroderma edule) reach maximum densities in soils with low lutum content,
while the opposite is true for Baltic tellins (Zwarts, 1988b). Through their effect on invertebrate prey
densities, sediment characteristics can be used to predict the densities of shorebirds (Yates et al.,
1993; van de Kam et al., 1999), and several studies point out that there is in fact a correlation between
sediment characteristics and shorebirds densities (e.g. Zwarts, 1988a; Yates et al., 1993; Holloway et
al., 1996; Moreira, 1999; Granadeiro et al., 2004; Clark, 2006; Granadeiro et al., 2006). These studies
have been conducted at large spatial scale (comparison of mean densities between estuaries) as well
as on a much smaller scale (within-estuary comparisons). Clark (2006) showed a positive correlation
between the mean proportion of silt and clay in the sediment and the density of Dunlins wintering in 14
estuaries in the UK. Holloway et al. (1996) compared bird densities in 27 estuaries (UK) and showed
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that in general estuaries on the east coast hold higher densities of birds, except for oystercatcher and
bar-tailed godwit. Estuaries along the east coast are generally muddier than the predominantly sandy
west coast estuaries (Yates et al., 1996). Geographical position may also explain a great deal of
variance in bird community, because this factor might be related to the proximity of breeding grounds
or position of flyways. At the same time, Yates et al. (1993) and Granadeiro et al. (2004 & in prep.)
found correlations between sediment type and shorebird density in within-estuary researches,
respectively in the Wash (UK) en the Tagus estuary (Portugal). Yates et al. (1993) showed that
densities of five species of shorebird correlated with at least one particle size category (proportion of
clay, silt, fine sand or coarse sand), however, correlation coefficients were generally low. Inclusion of
‘inundation period’ into the model, greatly improved its accuracy. In explaining shorebird distribution,
exposure time proved to be the most important factor in the Tagus. Here, sediment type only
explained 18.4 % of the variance, whereas exposure period explained 52.3% (Granadeiro et al.,
2006).
Sediment characteristics do not only influence prey densities, they also have an important effect on
prey availability. Sediment type can influence foraging behaviour in a very subtle way. An increased
sand content may result in a decrease of the time waders spent foraging there. This was found in an
experimental setup in Southern California involving dowitchers, western sandpipers, dunlins and
American avocets (Quammen, 1982). In an exclosure experiment, Quammen (1984) found that
shallow-feeding shorebirds reduced the density of prey by 26 to 80% at the muddiest mudflats, while
there was no effect on similar prey species (occurring in similar densities) in sandier mudflats. The
results of these experiments indicate that sand interferes with the detection and/or capture of prey
items that are similar in diameter to small sand grains (small oligochaete and polychaete worms),
resulting in lower intake rates.
Sediment type also correlates with the moisture content of the substrate, which in turn is of great
importance to prey availability (see §2.8).
2.3 Emersion time
2.3.1 Low tide counting bias
Low tide counts are generally adequate for comparison of total shorebird densities among estuaries
(Burton et al., 2004). However, they do not accurately reflect the relative importance of areas with
different exposure regimes (Nehls & Tiedemann, 1993; Blomert, 2002; Dias et al., 2006b; Granadeiro
et al., 2006). According to Dias et al. (2006b) estimates of bird densities across the intertidal area
based on low tide counts alone differ substantially from estimates based on repeated counts over the
full tidal cycle. High flats may favour high utilization intensity as they are accessible for a longer time
and birds concentrate there at high water levels. By contrast, low flats are accessible for a short period
during which the available area for birds is high. An equal exploitation of high and low flats is achieved
when birds restrict their feeding activities to the tide line. However if birds simply disperse with flowing
tide and concentrate with rising tide, a single survey at low tide would overestimate the utilization of
the lower parts of the tidal flats. If the birds stay in a preferred area (e.g. oystercatchers on a mussel
bed), a low tide survey may give a reasonable estimate even though the tidal utilization of high flats
where birds may have been feeding at higher water levels would be underestimated. Nehls &
Tiedemann (1993) thus divide the tidal foraging behaviour in three categories, namely ‘dispersed
foragers’, ‘tide line followers’ and ‘preferred area foragers’ (see Figure 2). In a study conducted by
Granadeiro et al. (2006), waders are divided into tide followers (black-tailed godwit, dunlin and avocet)
and non-followers (grey plover, redshank and bar-tailed godwit). Granadeiro et al. (2006) found that
the lower plots offered the highest rate of biomass acquisition. However, this did not compensate for
the much longer exposure period of the upper areas. The upper areas were much more important for
foraging waders since they provided the largest fraction of the biomass required by birds. There is,
however, poor agreement between various studies concerning classification of waders according to
their cyclic foraging behaviour as dictated by the tide (compare, for example, Thompson et al., 1986;
Nehls & Tiedemann, 1993; Tulp & de Goeij, 1994; van de Kam et al., 1999; Danufsky & Colwell, 2003;
Granadeiro et al., 2006).
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The recognition of the tidal behaviour of waders is thus crucial for the estimation of the exploitation of
tidal areas and studies aiming at forecasting shorebird densities across the intertidal habitat have to
take this into account (Dias et al., 2006b; Granadeiro et al., 2006).
c. preferred area
b. tide line
Exploitation
of intertidal area
Density at low tide
a. dispersed
high
low
high
low
high
low
Figure 2. Hypothetical distribution of birds at low tide representing three different feeding patterns (first row) and
results obtained by single low tide counts (second row) and repeated counts over the whole tidal cycle (third row).
(after Nehls & Tiedemann, 1993).
2.3.2 Emersion time as a predictor in bird distribution
The food present in an estuary is available to shorebirds only when shoals (flats surrounded by water)
and intertidal flats (flats alongside the estuary, connected to land) become exposed. An individual
wader must digest enough food to cover its daily energy need, if not, it loses fat, and consequently its
survival chances decrease (Stillman et al., 2005; Stillman & Goss-Custard, 2006). As the emersion
period determines the time intertidal flats are available to foraging shorebirds, it plays an important
role in the carrying capacity of an estuary.
Furthermore, the quality of an intertidal area is partly determined by its emersion period, since this has
a direct influence on prey distribution. In the Wadden Sea, biomass densities are highest at intertidal
areas with an emersion period of 3 to 5 hours (Zwarts, 1988b). Some benthic species can only forage
when submerged (filter feeders like cockle and mussel (Mytilus edulis)), while others have to wait until
the tide retreats (eg. Corophium, Scrobicularia plana). Filter feeders thus exhibit decreased growth
rates as the average submersion time decreases. Deposit feeders can continue feeding during low
tide, and are therefore expected to occur throughout the intertidal zone. The distribution of benthic
organisms, however, is only partly explained by the preference of each species for specific areas
within the tidal zone. Competitors and predators play a major role in their distribution. For example, the
presence of a mussel bed prevents the settlement of other benthic animals. Small larval animals are
likely to be sucked up by the filter feeding mussels. To a lesser extent the same is true for the
presence of lugworms (Arenicola marina), cockles or Scrobicularia plana. Apart from feeding on
similar foods and making it impossible for others to settle, some benthic animals prey on other benthic
species. The most important predators live in the water or on the sediment: fish, shorecrabs (Carcinus
maenas) and shrimps. Their predation pressure is highest where the crabs can stay longest: around
the low tide line. So although cockles can feed longer and grow more quickly near the low tide line,
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they are unlikely to survive here. Predation risk explains why cockles are rarely present where growing
conditions are optimal (van de Kam et al., 1999).
2.4 Drainage channels
Studies on habitat selection by waders in tidal flats have focused mainly on large-scale selection (e.g.
Goss-Custard, 1977; Moreira 1993; Piersma et al., 1993, Yates et al., 1993, Rosa et al., 2002). The
few studies that have analysed wader distribution at finer scales have documented strong responses
to microhabitat features, even at the scale of a few metres (Mouritsen & Jensen, 1992; Colwell &
Landrum 1993). Small drainage channels are the most obvious fine scale features in many tidal flats.
Some of these channels are formed directly by the drainage of the water that covers the flat during
high tide, but many have other origins, such as the drainage of adjacent saltmarshes, saltpans,
farmland and built-up areas (Lourenço et al. 2005).
Ravenscroft & Beardall (2003) showed significant higher numbers of redshank, dunlin and curlew in
the vicinity of freshwater flows. Important prey items of waders, like ragworm (Nereis diversicolor),
Corophium volutator and Hydrobia ulvae prefer organically rich areas (Hill et al., 1993; Yates et al.,
1993), and freshwater running off land adjacent to estuaries may increase local food abundance
through organic enrichment. This is countered by the fact that the flows in the study of Ravenscroft &
Beardall (2003) were derived from groundwater and were therefore unlikely to contain many nutrients.
A local effect on the salinity may enhance the presence of euryhaline species (Arenicola marina and
Corophium volutator). Where channels fan out over the lower and middle shores, the mudflat remains
wet at low tide. Waders prefer feeding on wet mudflats because this maintains the activity of
invertebrates and the penetrability of the substrate, which both enhance prey availability (see § 2.8).
In the Tagus estuary, Lourenço et al. (2005) showed that 44 % of the birds fed on just 12% of the
available surface less then 5 meter away from saltwater drainage channels. A study conducted by
Granadeiro et al. (2004) in the Tagus estuary shows that ‘distance to drainage channels’ is one of the
three most influential variables in modelling wader distribution in the Tagus estuary, followed by the
type of sediment and area of oyster beds. The channels in the Tagus estuary drain salt water,
originating from the adjacent saltmarshes and saltpans. There were significantly more shorebirds
(dunlin, grey plover, redshank, knot, bar-tailed godwit and black-tailed godwit) present close to the
channels. Shorebird densities peaked at about 1 to 2 meter from the edge of the channels. Moreover,
dunlin, grey plover and redshank had higher turning rates and lower step rates near the channels,
which indicates a higher foraging intensity. While characteristics of the sediments did not change
significantly with distance to the channels, prey abundance did, with Nereis diversicolor, Hydrobia
ulvae and Scrobicularia plana having higher densities and greater biomass closer to the channels. In
fact densities of Nereis diversicolor close to the drainage channels are particularly high, locally highest
ever found in the Tagus estuary (pers. comm. Pedro Lourenço). The reasons for the higher prey
density near the drainage channels are not clear, but may be related to food availability, larval
colonization or reduced heat loss in the presence of flowing water during low tide (Thrush, 1991;
Ravenscroft & Beardall, 2003).
The presence of drainage channels is thus very important for shorebirds since their presence enlarges
the carrying capacity and the overall quality of a mudflat. To maintain the quality of a mudflat, it seems
necessary to preserve the abundance of drainage channels. Tidal channels created by the action of
the tide are more abundant in wide intertidal flats (Leopold et al., 1993) so ideally large areas of flats
should be preserved. The drainage of saltmarshes is also responsible for the formation of channels on
the adjacent flats: mature saltmarshes result in more developed channel networks (Pye, 1992).
2.5 Salinity
Salinity has a major influence on the distribution and the abundance of macrobenthos, and in its turn
on prey availability, and thus on distribution of shorebirds (Wolff, 1969; Warwick et al., 1991; Colwell &
Landrum, 1993; Ysebaert et al., 2000; Ens et al., 2005). Ysebaert et al. (2000) showed a clear
zonation of the water bird communities along the entire salinity gradient of the Schelde estuary.
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Research in the Westerschelde revealed three abiotic variables that correlate significantly with wader
distribution, namely emersion time, salinity and current velocity (Ens et al., 2005).
2.6 Distance to high water roosts
In order to predict the ecological impact of human intervention in an estuary, one must keep in mind
that apart from the quality and quantity of intertidal habitat, the availability of high tide roosts plays an
important role. According to Rehfisch et al. (2003) there are four key criteria that determine whether a
roost is suitable or not:
•
•
•
•
Shelter from exposure
Proximity of foraging grounds
Minimal disturbance
Minimal predation risk
The cyclic flights between foraging grounds and high tide roosts involve a high energy expenditure to
shorebirds. The tendency to select feeding areas close to their roosts is a logical consequence of the
fact that wintering shorebirds may be subject to a critical energy balance. In general, wader densities
reach a maximum on the feeding areas close to the high tide roost because, when other
environmental factors remain equal, it is profitable to minimize the flight distance between the roost
and the feeding areas (Evans, 1976; Zwarts, 1981). Research in the Tagus estuary shows that there is
a significant decline in foraging dunlins further away from the roosts (Dias et al., 2006a). Although
Dias et al. (2006a) only studied dunlins they suggest a similar response for other waders, namely
redshank, turnstone, grey plover and oystercatcher. Based on research in the Wadden Sea, van Gils
et al. (2006) conclude that knots trade off energy intake rates against travel costs: sites near a roost
are skipped in case they offer low intake rates, while sites offering high intake rates are only used
frequently if roosting occurs nearby. In order to maintain the carrying capacity of an estuary, it is
important to maintain a network of favourably located high tide roosts (Dias et al., 2006a).
Apart from this, shorebird species differ in their fidelity to roost sites. While most species show strong
fidelity to high water roosts, knots, bar-tailed godwits and dunlins wintering in Scotland were found to
be highly mobile, showing poor fidelity to roost sites. These movements may be induced by reductions
in prey availability or by behaviour adapted to the likelihood of such problems occurring (Symonds et
al., 1984; Rehfisch et al., 2003). In this respect one should know that knots wintering in tropic areas
(North-western Australia and Mauritania) do show high roost fidelity (Leyrer et al., 2003; Rogers et al.,
2006). This clear difference in behaviour between tropical and temperate climate zones might result
from the fact that availability of prey is much more unpredictable in the temperate zones (Leyrer et al.,
2006).
In the Westerschelde, densities of shorebirds on the intertidal flats (flats alongside the estuary,
connected to land) are often (much) higher than on the shoals, even when sediment type and food
availability are equal. It is suggested that intertidal flats are more attractive to shorebirds because of
the shorter distance to high water roosts (Graveland, 2005).
2.7 Predators
Recently an increasing body of evidence has accumulated indicating that the feeding decisions of
shorebirds depend on the risk that they themselves are being eaten by predators (Cresswell, 1994a;
Hilton et al., 1999; Lank & Ydenberg, 2003; Whitfield, 2003; Ydenberg, 2004 van Gils et al., 2004; van
Gils et al., 2006).
In many circumstances there is a trade off between predation risk and the risk of starvation. For
example, higher predation risk while feeding (compared to the risk when resting) will make knots
feeding more efficient in order to reduce the time they are exposed to this threat (van Gils et al.; 2006).
When temperatures are low, metabolic costs increase, and simultaneously, the preparedness of
redshanks to accept higher predation risk in turn for greater intake rates increases, as found by Hilton
et al. (1999). Cresswell (1994a) in Tyninghame estuary, Scotland, reports that adult and juvenile
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redshanks segregated into two areas, namely a saltmarsh and a mussel bed. It was showed that a
redshank feeding in the saltmarsh was 4 to 8 times more likely to be killed, but had a higher foraging
rate and overall energy intake (1 to 7 times). Juveniles were excluded from the mussel beds by the
adults and Cresswell (1994a) thus concludes that adult redshanks prefer to minimize predation risk,
rather than to maximize intake rate. The adults could afford this because intake rate on the mussel
beds was sufficient to meet their daily energy requirements. However, one might expect that they will
abandon their mussel bed territories once intake rates fall below a minimum. Indeed, adult redshanks
appeared on the saltmarshes in late winter cold weather periods.
Whitfield (2003) showed how the distance from cover influences the vulnerability of waders to attacks
of Sparrowhawks. He found that the closer to cover they feed, the less waders are able to detect an
approaching raptor and escape in time. Hilton et al. (1999) report that when the visibility (e.g. because
of precipitation) decreased, redshanks used the more open (safe) areas. When feeding close to cover,
redshanks tend to forage in flocks (an effective anti-predation strategy), although this negatively
influenced feeding efficiency. On more open flats (far away from cover) birds had a less tendency to
flock, demonstrating once more the trade off between maximizing intake rate and minimizing predation
risk (Cresswell, 1994b; Whitfield, 2003).
In conservational view, it is important to know that predation risk partly determines the carrying
capacity. When different patches of an area differ in predation pressure, this may result in a different
usage of these patches by shorebirds. Thus, certain areas might be used more often than would be
expected based on “common” predictions (van Gils et al. 2004).
2.8 Prey availability
As already mentioned, prey availability is a key factor in determining shorebird distribution. In general,
prey availability correlates positively with prey density, but several other variables may be equally
important in determining how much of the food present on the flats is actually available to shorebirds.
Very important are the tidal changes in prey activity and accessibility (Smith & Evans, 1973; Evans,
1976; Evans, 1979; Puttick, 1979 & 1984; Pienkowski, 1983; Colwell & Landrum, 1993; van de Kam et
al., 1999; Ribeiro, 2004). Numbers of Nereis (Dugan, 1981) and Arenicola (Smith, 1975) visible at the
surface decline steadily after the tide has passed, in line with the drying out of the substrate.
Moreover, Nereis buries deeper after the tide has gone out. When the receding tide has just exposed
the flats, amphipods are very active, but from then on their activity steadily decreases. Therefore,
redshanks feeding on amphipods follow the receding water line (Boates, 1980; van de Kam et al.,
1999). The availability of polychaete worms like Scolelepis squamata also largely depends on the tidal
state. On Belgian beaches this worm occurs in a narrow zone at the high intertidal area (Degraer et
al., 2003). Scolelepis squamata is often presented as the preferred prey of sanderling (Dankers et al.,
1983; De Gee, 1984; Glutz von Blotzheim et al., 1984), but on Belgian beaches it seemed available to
sanderlings only a short period each tidal cycle, coinciding with the incoming tide crossing the zone
with high densities of worms. Most probably this is due to vertical migration of the worms throughout
the tidal cycle (De Meulenaer, 2006; Speybroeck et al., 2006). Kalejta & Hockey (1993) state that
rapid downward migration of prey following flat exposure is more likely in coarse sediments (beaches)
than in muddy environments, due to the lower water retention capacity of coarse sediments. The
wetness of the substrate affecting prey activity may partly explain why many waders follow the tide
line, though other factors may also be involved. Tactile foragers such as the knot use their sensitive
bill tip to locate invisible buried prey. Probing for prey, however, does not work in dry sand or liquid
mud, so tactile foraging knots are very much restricted to feed in moderately wet sediments (Piersma
et al., 1998). Furthermore, water content is positively correlated with sediment penetrability (Chapman,
1949; Perkins, 1958; Grant, 1984; Mouritsen & Jensen, 1992). Penetrability affects probing depth as
well as the cost of foraging in tactile searching birds (Myers et al., 1980; Pienkowski, 1981; Grant,
1984; Mouritsen & Jensen, 1992). Myers et al. (1980) showed a decrease in foraging success in
sanderling with decreasing sediment penetrability, owing to reduced probing depth. On a larger spatial
scale, Tjallingii (1972) found that the distribution of avocets was determined by the resistance of the
sediment to bill movements, rather than by prey density. Kelsey & Hassal (1989) have likewise
showed that dunlin preferred the wetter, low lying areas. The firmer ridges, with penetrability being
three times lower, attracted fewest birds, while the density of oligochaetes there was greatest.
9
Prey availability may vary seasonally due to variation in prey abundance as well as seasonal
differences in the behaviour (activity, burying depth) of benthic prey linked to temperature (Pienkowski
1981 & 1983; Puttick, 1984; Esselink & Zwarts, 1989; Nehls & Tiedemann 1993). For example, when
temperature drops beneath 6°C, Corophium volutator, a favoured prey of redshank, becomes less
active and the birds take increasing numbers of Baltic tellin or Nereis diversicolor (Goss-Custard,
1969). In other words: changes in temperature can influence prey choice of shorebirds and may thus
affect the spatial distribution of birds. Many intertidal organisms move to greater depths within the
sediment as temperature drops (Esselink & Zwarts, 1989). At temperatures just above freezing point,
annelids and bivalves are buried in the sediment at a depth of more than 15cm and are therefore even
out of reach of a curlew’s bill. Apart from vertical migration, there is evidence that marine invertebrates
may move to lower tidal levels in response to cold weather (Darby, 1975; Evans, 1979). Similarly, high
temperatures and strong winds that dry out the substrate may reduce prey availability for waders as
benthic prey moves deeper to avoid desiccation (Evans, 1976).
Since good feeding areas attract many foraging birds, this is likely to promote intra- and interspecific
interference. In early spring, the total numbers of oystercatcher in the Oosterschelde (NL) are lowest,
and only the richest foraging areas are occupied. When numbers rise however, the densities increase
to a ceiling level, and from this point on densities in other (less profitable) foraging areas start to
increase (Meire, 1993). Interference can be associated with prey depletion and/or disturbance,
restriction of the field view and kleptoparasitism (eg. Goss-Custard, 1980 &1985; Zwarts, 1981;
Thompson, 1986; van de Kam et al., 1999; Stillman et al, 2003, 2005; Stillman & Goss-Custard,
2006). Studies on the amphipod Corophium volutator showed that these invertebrates retreat into their
burrows when a wader passes (Goss-Custard, 1970). Therefore, at high densities of shorebirds
amphipod availability decreases quickly. For that reason redshanks feeding on amphipods will occur
rather dispersed across the intertidal area. This is in contrast to knots, feeding in large high density
groups. Knots can afford this because their presence does not repress the availability of buried Baltic
Tellin. Moreover, feeding in large flocks offers advantages in terms of protection against predators, or
in finding good foraging spots (van de Kam et al., 1999).
2.9 Shoal morphology
The morphology of shoals present in an estuary may largely determine the carrying capacity of the
estuary for shorebirds. Obviously, it determines the area of intertidal habitat that is available to staging
waders. Moreover, the height of the shoals determines the time they are exposed and the availability
of the shoal throughout the tidal cycle. To a lesser extent habitat quality is dictated by shoal
morphology. The shape and location determine the prevailing dynamics, which correlate strongly with
the sediment composition. For example, in the Westerschelde there is a positive correlation between
the height of the shoal and the high tide current velocity. Consequently, there is a positive correlation
between the height of the shoal and the coarseness of the soil sediments (Brinkman et al., 2005). At a
smaller scale, dynamics vary within the shoal, and shoal-edges exposed to high currents are steeper
and show ripples, and these edges are considered to be the most dynamic parts of the shoal.
However, highest densities of benthic prey are found at low-dynamic intertidal habitat (Pieters et al.,
1991, Vroon et al., 1997).
Hence, if widening the shipping channel in the Westerschelde results in higher shoals, the sediment is
expected to become muddier. At the same time, emersion periods increase and the shoals become
available to foraging waders for a longer period. However, if the shoals grow above the mean high
water level, they are no longer attractive as a foraging area to waders, but they may function as a
breeding habitat for terns and plovers, or as a high tide roost for waders. In this respect, connection
channels play an important role in maintaining enough dynamics to prevent shoals from growing
above the mean high water level. Due to the presence of connection channels, there is more diversity
in microhabitats, plus, the area of intertidal is more extensive. In the Westerschelde, there is a longterm evolution going on in the disappearance of connection channels. In the middle and the west of
the estuary this is probably the result of natural processes, but in the east the disappearance of
connection channels is thought to be linked to the channel widening in the early seventies (Vroon et
al., 1997). Through widening of the shipping channel, the tide wave experiences less resistance
entering and leaving the estuary. Hypothetically spoken this might result in a rise of the high water
level and hence stronger dynamics above the shoals.
10
At the end of the eighties, the project OOSTWEST was started up as a result of the concern that
human intervention would have a negative effect on the estuary. After the final report ‘Westerschelde:
stram of struis?’ in 1995, two parallel projects, namely ZEEKENNIS and MOVE were started up. The
monitoring project MOVE aimed at evaluating the effect of the widening of the shipping channel in
1996 (48’/43’), and the project ZEEKENNIS at enlarging the insight in the physical and ecological
functioning of the Westerschelde. Concerning morphological changes, it is often very difficult to detach
ongoing long term trends from short term trends, or to distinguish natural changes from changes
induced by human intervention. Nevertheless, based on the results of the ten-year monitoring
programme MOVE, the following changes in the overall morphodynamics of the Westerschelde have
taken place. Mean high water levels have not risen since the previous channel widening, but low water
levels have decreased. No significant changes in current velocity have been observed, apart from
some very local changes near shoal sides and at dump locations. Shoal area in the west and east of
the Westerschelde has decreased following the long term trend as observed in the last fifty years. In
the middle part of the estuary the shoal area has decreased even more than was expected. Most of
the shoal area has been transformed to ‘shallow water’, because of erosion of the shoal sides. This
phenomenon is most probably caused by the channel widening. In the Westerschelde as a whole, low
dynamic intertidal area has increased, and high dynamic intertidal area has decreased. With respect
to the ecological function of the estuary for waders, this is a positive evolution since benthic prey
organisms prefer low dynamic habitat (van Eck, 2006).
11
12
3 SPECIES: HABITAT DEMANDS
For each species an overview is given of the existing knowledge concerning its habitat demands. The
emphasis is on the preferred sediment characteristics and the effect of emersion time on bird
densities. Please keep in mind that the effect of emersion time on wader densities very much depends
on the way birds were counted. For example, while most studies use low water counts only, Ens et al.
(2005) used bird count data obtained by repeated counts (each ½ hour) over the whole of the
exposure period. Counts conducted during low tide only tend to underestimate the importance of high
intertidal areas (see § 2.3.1). Furthermore, if available more information is given concerning specific
habitat demands, the species’ mobility throughout estuaries, nocturnal foraging habits and inland
foraging. These factors greatly determine the species flexibility to cope with extreme conditions, and
are important towards a correct estimation of the carrying capacity of a certain area. Finally, each
species’ diet is discussed, and the effect of the distribution and tidal behaviour of the prey on the
foraging behaviour of the birds is considered.
3.1 Oystercatcher (Haematopus ostralegus)
There is good agreement in literature concerning the habitat choice of oystercatchers. This species
generally prefers sandy soils for foraging. In Guinea-Bissau, the oystercatcher comes second in row
after sanderling in a ranking of 15 wader species according to their preference from sandy to muddy
sediments (Zwarts, 1988a). In the Wash (UK), oystercatcher densities correlate positively with the
area of sand, as well as with the proportion of fine sand (63-125µm) in the sediment, and correlate
negatively with the silt content (20-63µm) (Goss-Custard & Yates, 1992; Yates et al., 1993).
Comparing densities of oystercatchers in 27 British estuaries showed that highest densities occurred
in the less muddy estuaries with a high degree of wave action and exposure to swell (Austin et al.,
1996). Hierarchical classification of 109 British estuaries based on their wader communities revealed
four groups. The group containing the larger, sandier estuaries, held highest densities of knot, bartailed godwit, sanderling and oystercatcher, as found by Hill et al. (1993). Research in the Netherlands
shows that oystercatchers in the Westerschelde occur on a broad range of sediments (Van Kleunen,
1999 (Appendix I); Ens et al., 2005), while in the Wadden Sea they show a preference to the less
muddy areas (Brinkman & Ens, 1998). This is confirmed by Figure 3, which is based on the same data
as the report of Brinkman & Ens (1998) (Zwarts, unpublished data, in: Blomert, 2002).
0,500
0,500
0,400
0,400
wader density (n/0,1ha)
wader density (n/0,1ha)
In the Wadden Sea, meadows along the mainland coast and on the islands are sometimes used as
feeding grounds, mainly during bad weather when exposure time of the flats is too short, or during
cold winter periods when energy requirements are higher (Smit & Wolff, 1981).
0,300
0,200
0,100
0,300
0,200
0,100
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
Figure 3. Relation between densities of oystercatcher and the lutum content of the substrate (left) and emersion
period (right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002)
In the Westerschelde, oystercatchers occur over a wide range of emersion periods (Van Kleunen,
1999 (Appendix I); Ens et al., 2005), whereas in the Wadden Sea they typically occur in areas with
rather short emersion times (Brinkman & Ens, 1998; see Figure 3). Comparatively, Smit & Wolff
(1981) state that oystercatchers favour areas that are exposed for 0-6 hours. Meire (1993) describes
13
the tidal behaviour of oystercatchers in the Oosterschelde (NL). Cockles and mussels are the most
important prey species, and are not uniformly spread over the tidal flats, but occur on the lower
intertidal zone. As the tide ebbs, the birds tend to follow the waterline to reach the lower richer feeding
areas as soon as possible. This results in a clear peak of birds moving through the plots in the higher
tidal zones, while these plots are nearly abandoned near low tide. When the preferred feeding areas
below mid tidal level become exposed, birds occur there in constant high densities until they are
flooded again. This tidal behaviour corresponds with the ‘preferred area’ behaviour as described by
Nehls & Tiedemann (1993) (see Figure 2).
During winter, oystercatchers feed nearly exclusively on shellfish, especially cockles and mussels, but
also other larger shellfish species like Baltic tellin, Mya arenaria and Scrobicularia plana. In summer
Nereis is also eaten, mainly by females (eg. Hulscher, 1996; Zwarts et al., 1996b). In the
Westerschelde, cockles are the most important prey, since mussel beds are rare (Van Kleunen, 1999;
Ens et al., 2005). Cockles typically occur in soils with rather low lutum content, and intermediate
exposure periods (Zwarts, 1988b, grafiek in: van de Kam et al., 1999). According to Smit & Wolff
(1981), the majority of oystercatchers in the Wadden Sea concentrates on the mussel beds and cockle
fields, or on places with concentrations of Mya arenaria and Scrobicularia plana. Studies in the UK
and the Netherlands indeed show a strong association of oystercatcher to mussel beds (Ens et al.,
1993; Yates et al., 1993). There are, however, always small numbers feeding on tidal flats
characterised by Arenicola marina, where Arenicola, Nereis and Baltic tellin are eaten (Smit & Wolff,
1981).
Meire (1993) states that without a detailed knowledge of the foraging behaviour of the predator, it is
not possible to give an adequate estimate of the harvestable prey density, which in turn is essential to
calculate the carrying capacity of a given area. In this respect, Hulscher (1996) found that
oystercatchers reject mussels smaller than 20-25 mm in length because of low profitability, and take
all larger size classes in proportions conform to the likelihood of encounter. The profitability of
hammered mussels decreases when they are larger than 50-55 mm because some of these cannot be
opened at all, and time is spent in failed attacks. As a result, the profitability curve shows a peak for
mussel lengths around 50-55mm (Meire, 1993). When foraging on cockles, oystercatchers refuse first
year cockles smaller than 10mm when older cockles are present (Sutherland, 1982).
The average mussel length taken by oystercatchers in the Oosterschelde (NL) is 30-45mm (Meire,
1993). The results obtained by Meire (1993) can well be understood within the framework of the
optimal foraging theory (birds maximizing their intake rate at all times) when availability of the different
mussel length categories is taken into account. Moreover, oystercatchers select mussels with thin
shells, since the mean shell thickness of mussels opened by oystercatchers is less than that of the
mussels present.
Goss-Custard et al. (2004) modelled five major estuaries in the United Kingdom and France (Exe,
Wash, Bangor flats, Burry Inlet, Baie de Somme). They concluded that between 2,5 and 7,7 times the
shellfish biomass that is actually consumed, must be available in autumn if most birds are to survive
until spring. Main reason here for is that by reducing the biomass of shellfish available per bird,
interference competition for food is intensified.
When oystercatchers are unable to take in enough food during the day, they will feed at night as well.
Zwarts et al. (1996b) found that oystercatchers feeding on Baltic tellin and Scrobicularia plana began
feeding at night after these bivalves migrated deeper into the soil in the course of autumn. Several
studies appear to contradict each other when it comes to nightly foraging success (Hulscher, 1996).
Zwarts & Drent (in: Smit & Wolff, 1981) suggest that the intake rate of mussels during night is only half
compared to day time intake rate. Sutherland (1982) states that oystercatchers switched from visual
detection of prey during day time to tactile feeding at night, and in doing so, found cockles of smaller
size, at a lower rate than they did during the day. By contrast, under controlled conditions Hulscher
(1976) found that oystercatchers reached a higher intake rate at night using tactile foraging
techniques. Probing for food, however, is energetically more expensive, and in this study the net
energy intake could not be evaluated.
14
3.2 Avocet (Recurvirostra avosetta)
The avocet strongly prefers the most muddy sediments for foraging. Research in the Netherlands
showed a preference of avocet to muddy areas in the Delta area (Wolff, 1969; Van Kleunen, 1999;
see Appendix I) and a strong positive correlation with the area of muddy (high) intertidal zones in the
Wadden Sea (Ens et al., 1993). Looking at Figure 4, one sees that in the Wadden Sea, avocets occur
nearly exclusively on sediments with a lutum content of 5% or more. In the Tagus estuary, the avocet
exclusively forages on mud and sandy mud, and of all wader species present, avocets (and blacktailed godwits) feed on the finest sediments (Moreira, 1999). A study conducted in Humboldt Bay,
California, showed a negative correlation of American avocet with sediment particle size, with birds
occurring nearly exclusively in areas of fine sediment (Evans & Harris, 1994; Danufsky & Colwell,
2003). At a larger spatial scale, a DCA-analysis of 109 estuaries (UK) according to their wintering
shorebird communities, revealed that avocets reach highest densities in the very muddy estuaries and
coastal lagoons (Hill et al., 1993).
Increasing the sand content of the substrate from 2 to 14% showed that sand interferes with the
detection and/or capture of prey (Quammen, 1982). This could be deducted from the fact that the time
spent in the treated plots decreased, and avocets started pecking at the surface in addition to
‘scything’ (see below), the more common way of feeding. Tjallingii (1972) reported that the resistance
of the soil to the bill movements determines the spatial distribution of foraging birds more than density
of their prey did.
0,005
0,010
0,004
0,008
wader density (n/0,1ha)
wader density (n/0,1ha)
In the Wadden Sea, the density of avocets in relation to emersion time shows two peaks: one at short
emersion periods (4 hours) and one at higher emersion periods (6,5 hours) (Figure 4). Overall
densities in the Wadden Sea being very low, this may enhance unreliable results. Other research in
the Wadden Sea showed a strong positive correlation between avocet densities and the area of high
intertidal zones (Ens et al., 1993). Studies conducted at the Tagus estuary also report a positive
correlation between densities of avocet and the exposure period, with avocets being more numerous
on the higher reaches of the intertidal area, mainly consisting of muddy sediments retaining a thin
layer of water (Moreira, 1995; Granadeiro et al., in press). On the other hand, Granadeiro et al. (2006)
classifies avocet as being a follower, suggesting a preference to the lower intertidal. Evans & Harris
(1994) describe the intertidal behaviour of wintering American avocets in Humboldt Bay, California.
There, most birds seem to follow the retreating tide edge, while a few birds always remained on the
higher exposed mudflats containing visible surface water. Avocets foraging on the intertidal mudflats
mostly waded in water covering their feet (43%), in water up to belly (34%), or walked on mudflats with
visible surface water (22%). In coastal lagoons in Ghana, avocets favour water depths of 2-11 cm
(Ntiamoa-baidu et al., 1998).
0,003
0,002
0,001
0,006
0,004
0,002
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
Figure 4. Relation between densities of avocet and the lutum content of the substrate (left) and emersion period
(right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002).
In the Wadden Sea, Nereis diversicolor was found to be the most important food item for avocets. The
same was found for the Ventjagersplaten in the Delta area. Other small prey like Corophium and
insects complete the diet. Locally, avocets feed in brackish channels on small crustaceans
(Paleomonetus and Neomysis) (see literature review in Leopold et al., 2004). Avocets use their
15
upward curved bill for a characteristic way of (tactile) feeding: while walking through shallow water or
soft sediment, they quickly sweep their bill through the top layer of the silt or the water (scything)
(Tjallingii, 1972). Avocets also peck for prey visible in clear water, on the sediment or amongst the
vegetation on the edge of the water. They sometimes forage in dense flocks hunting for crustaceans
(shrimps, mysidacea), often accompanied by other species like spotted redshank (Ntiamoa-baidu et
al., 1998; van de Kam et al., 1999).
Boettcher & Haig (1995) showed that in South island, South Carolina, impoundment use by American
avocet is far greater than intertidal mudflat use. There, avocets invariably used areas covered by
shallow water (5-17 cm) with little or no exposed substrate. Evans & Harris (1994) found that avocets,
who normally forage at intertidal mudflats during low tide, occasionally fed exclusively at oxidation
ponds taking advantage of large but variable availability of Daphne magna.
Several authors point out that night feeding can be very important. In (non-tidal) coastal lagoons in the
gulf of Guinea (Ghana), avocets probably forage more during night time (Ntiamoa-baidu et al., 1998).
American avocets in Humboldt Bay, California, are also presumed to forage effectively during night
time, since the birds use primarily tactile feeding methods and were observed feeding in the same
locations as during daytime (Evans & Harris, 1994). Hötker (1999) studied time activity budgets of
avocets and reports that activity pattern in estuarine areas was mainly influenced by the tide. Activity
patterns by day and at night were essentially the same, except during very dark nights, when foraging
activity was reduced. By contrast, Zwarts et al. (1990) observed daytime feeding only, in a non-tidal
lagoon in Senegal.
Evans & Harris (1994) report that nearly all American avocets foraged within 3 km of the roosts.
16
3.3 Ringed plover (Charadrius hiaticula)
In general, ringed plovers are encountered on intermediate to muddy substrates. In the
Westerschelde, highest densities occur on intermediate substrate (Ens et al., 2005). In the Wadden
Sea, their habitat preference appears to be segregated according emersion period: ringed plovers
favour intermediate sediments at the higher intertidal zones, while they prefer muddy sediments at the
lower tidal flats (Brinkman & Ens, 1998). Looking at Figure 5, densities of ringed plovers in the
Wadden Sea in relation to lutum content of the sediment show two distinctive peaks, one on sandy
and one on muddy substrates. When the data are further analysed, it appears that in areas with a long
emersion time, the preferred sediment is muddy, and in areas with shorter emersion times, favoured
sediment is sandy (Figure 6). This is the opposite of what is stated in Brinkman & Ens (1998)! Out of
15 species of shorebirds wintering in Guinea-Bissau, ringed plover showed the strongest association
to muddy sediments (Zwarts, 1988a). In the Tagus estuary, Moreira (1999) found a preference for
sandy mud, while muddy as well as coarser sediments were clearly avoided. However, through a
cluster analysis, Granadeiro et al. (in press) distinguished four wader communities, in which ringed
plover was associated with Kentish plover, Greenshank, knot and turnstone due to their preference to
the less muddy sediments.
Danufsky & Colwell (2003) state that plovers are non-followers, probably to avoid inter- and
intraspecific concurrence. Smit & Wolff (1981) report that ringed plovers primarily feed on the high
eulittoral, and even on the supralittoral zones. Brinkman & Ens (1998) and Ens et al. (2005) also found
a preference for higher parts of the intertidal zone, respectively in the Wadden Sea and the
Westerschelde. Looking at Figure 5, ringed plovers in the Wadden Sea reach highest densities on
mudflats with long emersion periods. However a secondary peak density occurs at the lower intertidal
zone.
0,016
0,008
wader density (n/0,1ha)
wader density (n/0,1ha)
0,010
0,006
0,004
0,002
0,012
0,008
0,004
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
lutum content (%)
Figure 5. Relation between densities of ringed plover and lutum content of the substrate (left) and emersion
period (right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002).
wader density (n/0,1 ha)
0,06
0,05
0,04
0,03
0,02
0,01
0
<0,5
.5-1.5
1.5-3.0
3-5
lutum content (%)
5-8
8-12
12-18
emersion time 5u
emersion time 7u
Figure 6. Relation between densities of ringed plover and the lutum content of the substrate, after segregation
according to emersion time (after Zwarts, unpublished data, in: Blomert, 2002).
17
Nereis diversicolor is often mentioned as the most favoured prey item of ringed plovers. Along the east
coast of the UK, the species mainly feeds on thin worms (Scoloplos and Notomastus). Other prey
mentioned in literature involves insects, amphipods, Hydrobia and Carcinus maenas. Bivalves have
never been found as prey (see literature review by Leopold et al., 2004).
Ringed plovers forage almost entirely by visual means, so they greatly depend on the activity pattern
of their prey. For example, capture rates are positively correlated to sand temperature (increased prey
activity), and inversely related to wind force (decreased activity through desiccation of the substrate)
(Pienkowski, 1981 &1983). This only applies when air temperature is fairly low. When air temperature
is higher, capture rates decline again despite continuing increase in prey activity. Mean prey size
increased however, so it is likely that the plovers become more selective for larger prey when prey
availability increases. In situations of low availability, ringed plovers are reported to induce activity
through ‘foot vibration’, which leads to an increase in activity of small crustaceans (Pienkowski, 1981 &
1983). As discussed above, ringed plovers in the Wadden sea favour the muddiest sediments when
foraging on the high intertidal (see Figure 6). This seems logical, since prey activity correlates
positively with the moisture content of the sediment (see §2.8), and muddy soils have a higher water
retention capacity compared to coarser soils. It could however also be the other way around, since
sandy flats are often characterised by surface pooling, while muddy flats are often convex and water
runs off more quickly (pers. comm. Bruno Ens).
Despite being a visual forager, a high degree in night time foraging is reported by Ntiamoa-baidu et al.
(1998) in coastal lagoons in Guinea-Bissau. In the Berg River estuary, South Africa, Kalejta (1992)
found a ratio of night to day foraging numbers of Charadrius spp. of 2,85. On the other hand, Zwarts et
al. (1990) reports a clearly lower feeding activity at night, since densities at night are but a fourth of
feeding densities during daytime. According to Pienkowski (1982), the peck rate of ringed plovers
during night time is about half of that during the day. However, feeding success and prey size could
not be measured, so they might achieve higher intake rates when larger prey would come available at
night (see §3.5).
18
3.4 Kentish plover (Charadrius alexandrinus)
Little was found on the habitat preference of foraging Kentish plovers. In Guinea-Bissau the Kentish
plover reaches highest densities on sandy mud and soft mud, and takes 10th position in a ranking of
15 wader species according to their sediment preference from sandy to muddy (Zwarts, 1988a). In the
Tagus estuary, Kentish plovers occur nearly exclusively on sandy muds (Moreira, 1999), but show a
negative correlation to the mud content according to Granadeiro et al. (2004). Also at the Tagus
estuary, Granadeiro et al. (in press) distinguished four wader communities, in which Kentish plover
was associated with ringed plover, Greenshank, knot and turnstone, a community that is said to favour
the less muddy sediments.
According to Smit & Wolff (1981), Kentish plovers in the Wadden Sea use shallows in the higher
eulittoral or supralittoral. Compared to ringed plovers, they prefer moister substrates, and are more
often found on the intertidal flats. In general, plovers are non-followers, preferring the higher reaches
of the intertidal (Danufsky & Colwell, 2003). Perez-Hurtado (1997) found that in Cadiz Bay, Spain,
Kentish plovers were mainly foraging in the marshes and saltpans with low water levels adjacent to
the intertidal mudflats.
Cramp & Simmons (1983) state that polychaete worms, molluscs and crustaceans are important prey
in coastal and inland saltwater areas. In Schleswig-Holstein stomachs of six birds contained insects
and their larvae, crustaceans (Carcinus maenas), Nereis, gastropods (Hydrobia, Littorina) and a
bivalve (Lange, 1968; Höfmann & Hoerschelmann, 1969). Dropping analysis in southwest Spain
showed larvae of diptera and coleoptera (Perez-Hurtado, 1997). Kentish plovers forage in the typical
plover’s “stop-run-peck”-mode.
They have not been observed feeding by night by Zwarts et al. (1990) in Mauritania, Banc d’ Arguin.
19
20
3.5 Grey plover (Pluvialis squatarola)
0,020
0,020
0,016
0,016
wader density (n/0,1ha)
wader density (n/0,1ha)
In general, grey plovers occur on a broad range of sediment types, but appear to favour muddy
sediments. In the Wadden Sea, grey plovers exploit sandy as well as muddy tidal flats, and also occur
on the mussel beds and cockle fields (Smit & Wolff, 1981). Brinkman & Ens (1998) state that highest
densities in the Wadden Sea are found on intermediate sediments. Figure 7 and Figure 8 show more
detailed information of the Wadden Sea, in which appears that grey plovers occur on a broad range of
sediments with two peak densities: one on muddy, and one on rather sandy sediments. When the data
are segregated according to emersion time, the same two folded habitat preference as found in ringed
plover appears: in areas with high emersion times, muddy sediments are preferred, but in low intertidal
areas densities are highest on the more sandy substrates. In the Westerschelde, Ens et al. (2005)
scored the preferred habitat as muddy. According to the graphs presented by van Kleunen (1999),
grey plovers in the Westerschelde occur in maximum densities in the muddiest areas, but there is also
a second lower peak at sandy sediments (see Appendix I). In the Wash (UK), Goss-Custard & Yates
(1992) found a positive correlation between grey plover densities and the area of mud. By contrast,
Yates et al. (1993) showed a negative correlation between grey plover density and the silt content (2063µm) of the sediment. In Guinea-Bissau, grey plovers occur on the somewhat muddier areas
(Zwarts, 1988a). In the Tagus estuary, several studies point out that grey plovers prefer the muddier
sediments. According to Moreira (1999) grey plovers occur nearly exclusively on sandy mud and
muds, with a clear optimum on sandy muds. Granadeiro et al. (2004) found a positive correlation
between bird densities and the mud content of the sediment. Furthermore, Granadeiro et al. (in press)
report that high densities of grey plovers coincide with high densities of dunlin, redshank and bar-tailed
godwit, a wader community with strong preference to muddy substrates.
0,012
0,008
0,004
0,012
0,008
0,004
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
lutum content (%)
Figure 7. Relation between densities of grey plover and the lutum content of the substrate (left) and emersion
period (right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002).
wader density (n/0,1 ha)
0,02
0,016
0,012
0,008
0,004
0
<0,5
.5-1.5
1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
emersion time 4u
emersion time 7u
Figure 8. Relation between densities of grey plover and the lutum content of the substrate, after segregation
according to emersion time (after Zwarts, unpublished data, in: Blomert, 2002).
Grey plovers are regarded as non-followers (Townshend et al., 1984; van de Kam et al., 1999;
Granadeiro et al., 2006). Being a typical visual forager (Pienkowski, 1983), this is an expected result,
since followers are generally tactile foragers (Granadeiro et al., 2006). In the Wadden Sea, grey
21
plovers show peak densities in areas with intermediate emersion periods of 5,5 hours (see Figure 7),
while Brinkman & Ens (1998) report a preference to the high intertidal. In the Westerschelde, van
Kleunen (1999) showed that grey plovers occur in high densities at high intertidal areas (emersion
period of 60-100%) as well as on low intertidal areas (emersion time 0-25%) (Appendix I). Ens et al.
(2005) report a preference to high intertidal areas in the Westerschelde. Others studies, in the Wash
(UK) and the Tagus estuary (Portugal), show a negative correlation between grey plover densities and
the emersion period (Yates et al., 1993; Granadeiro et al., 2004).
The greater part of prey items caught by grey plovers consists of large worms (Arenicola, Nereis), but
smaller worms (principally Notomastus) can also be a very important food source. Small cockles,
mussels and Baltic tellins have also been noticed, mainly in the Wash estuary. Crustaceans are
largely absent in the species’ diet (Pienkowski, 1982; see also literature review by Leopold et al.,
2004).
Grey plovers strongly depend on the activity of their prey, and as in ringed plovers, capture rates are
related to sand temperature, wind force and rainfall (Pienkowski, 1981 & 1983). Furthermore,
Pienkowski (1983) found an inverse relationship between the capture rates of small and of large
worms, so the rate of capturing thin worms was depressed when the rate of taking Arenicola
increased. The observations confirmed that grey plovers actively select the larger Arenicola (greater
calorific value), obeying the optimal foraging theory. Thus, when falling temperatures or increasing
time after high water cause a decrease in Arenicola activity, more thin worms were taken. This causes
a shift in food source during each tidal cycle. Desiccation of the substrate also influences prey activity.
In the Berg River estuary, South Africa, the species is most abundant on the intertidal areas with most
vegetation cover. Kalejta & Hockey (1993) suggest that this is caused by the fact that the vegetation
cover reduces the rate of mudflat desiccation during exposure. Reduced desiccation in muddy areas
may also explain why grey plovers foraging on the high intertidal favour the muddiest areas as shown
in Figure 8.
Pienkowski (1981 & 1983) states that the tidal behaviour of grey plover is partly influenced by the
presence of bar-tailed godwits. Being a visual forager, grey plovers acquire a large area available to
each bird, and are excluded by the tactile foraging godwits that are able to forage efficiently in high
density groups. After departure of the godwits in spring, grey plovers spread nearer to the tide edge
where prey availability is highest.
Night foraging is reported by several authors (Pienkowski, 1980 & 1982; Dugan, 1981; Zwarts et al.,
1990; Kalejta, 1992; Ntiamoa-baidu et al., 1998). Kalejta (1992) found a mean ratio of night to day
foraging numbers of 0,72 from December until March in the Berg River estuary, South Africa. The ratio
night/day density during premigration period amounts to 0,69 as found by Zwarts et al. (1990) in Banc
d’ Arguin, Mauritania. According to Pienkowski (1982), the peck rate of grey plovers during night time
is about half of that recorded during the day, and Kalejta (1992) also found grey plovers to forage
significantly slower at night. However, this does not necessarily mean a decrease in intake, since
feeding success could not be measured in these studies. In this respect, Pienkowski (1980) showed a
marked increase in Nereis-availability during night time, which may compensate for the decrease in
foraging rate. Dugan (1981) found that grey plovers change their feeding site at night, and probably
also changed diet from Nereis diversicolor to the much larger Nereis virens. He suggests that the
major part of the energy requirements of some individual grey plovers are met at night rather then by
day.
According to Lourenço et al. (2005), grey plovers show strong association to intertidal drainage
channels.
22
3.6 Knot (Calidris canutus)
In general, knots seem to prefer intermediate sediments, with slightly differing results obtained by
several studies. In the Westerschelde, knots were found to prefer intermediate substrates (van
Kleunen, 1999 (Appendix I); Ens et al., 2005). According to Smit & Wolff (1981), preferred feeding
areas in the Wadden Sea vary from place to place, but slightly muddy tidal flats and mussel beds are
favoured most. Figure 9, based on low tide counts in the Wadden Sea, shows avoidance of the most
sandy sediments, and a preference for intermediate substrates with lutum content between 1,5 to 5%.
At the shores of the Wash, Goss-Custard & Yates (1992) found that densities of knots correlate
positively with the area of sandy substrate. However, sediment characteristics in this study were
assessed using satellite imagery. In a more detailed study including soil sampling, Yates et al. (1993)
found a positive correlation between density of knots and the proportion of fine sand (63-125µm), but
equally so with the proportion of silt (20-63µm) in the sediment. In defining four groups of estuaries
based on their wader communities, Hill et al. (1993) found that high densities of knot coincide with
high densities of sanderling, bar-tailed godwit and oystercatcher in the larger, sandier estuaries. In
Guinea-Bissau, knots reach highest densities on muddy sand, and end up 4th in a ranking of 15
species of shorebird according to their habitat preference from sandy to muddy sediments (Zwarts,
1988a). In a similar ranking of 13 species of wader in the Tagus estuary, the knot takes in an
intermediate position, favouring sandy muds (Moreira, 1999).
0,100
0,100
0,080
0,080
wader density (n/0,1ha)
wader density (n/0,1ha)
Little was found concerning the relation between densities of knot and the emersion period. According
to Goss-Custard (1977), knots do not follow the tide line once their preferred feeding areas are
exposed. Such tidal behaviour (‘preferred area’, see Figure 2) is described by Nehls & Tiedemann
(1993). The modelling of wader distribution in the Westerschelde and the Wadden Sea showed a
preference for intermediate emersion periods (Brinkman & Ens, 1998; Ens et al., 2005).
0,060
0,040
0,020
0,060
0,040
0,020
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
Figure 9. Relation between densities of knot and lutum content of the substrate (left) and emersion period (right),
based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002).
Knots use their sensitive bill tip to locate invisible buried prey. The efficiency of this tactile foraging
depends on the water content of the sediment, and this mechanism does not work in dry sand, nor in
liquid mud, so knots are only found foraging on moderately wet sediments (Piersma et al., 1998).
Knots show a strong preference for bivalves (especially Baltic tellin and small cockle and mussel).
Worms lack nearly completely in their diet, which makes the knot unique in the range of waders
studied here (see literature review by Leopold et al., 2004). When birds arrive from the arctic they
have small gizzards and rely heavily on soft bodied prey for some time. In July and August, knots
arriving at the Wadden Sea thus take advantage of great abundance of crustaceans (Crangon
crangon and young Carcinus maenas). Crustacean densities rapidly decline, and knots switch to their
normal bivalve prey, while their gizzards grow larger to cope (van Gils et al., 2005b).
Most shorebirds behave according to the contingency model, which implies that the birds spend all
their time foraging (handling and searching), and that their maximum energy intake rates are
constrained by the rate at which prey can be externally handled (cfr. oystercatcher, Meire, 1993).
Knots however ingest their shelled prey as a whole, which is subsequently crushed in the gizzard. A
knot obeying the contingency rules, maximizing its energy intake per unit foraging time, does not
23
necessarily maximizes its intake per total unit of time (foraging plus digestive pauses). Therefore, it is
expected that knots are selective towards prey that is rapidly digested, so time that would be lost to
digestive pauses can be used to search for easy-to-digest prey. Experimental tests conducted by van
Gils et al. (2005a & 2006) indeed shows that knots obey the ‘digestive rate model’ much more than the
‘contingency model’.
Knots show a tremendous flexibility (inter- and intra-individual variation) in digestive organ size
(Piersma et al., 1993b; van Gils et al., 2003), and it has also been verified that gizzard size constrains
digestive processing rate in knots (van Gils et al., 2003). This influences the patch choice as shown by
van Gils et al. (2005b). Comparing two contrasting patches, the patch with high densities of hardshelled prey attracted birds with large gizzards, while the patch with low densities of soft-shelled prey
attracted birds with smaller gizzards. Birds with small gizzards are even forced to extend their foraging
time beyond the 12 hour tidal system. This is possible because in the Wadden Sea, there are large
spatial differences from west to east in the timing of the tidal cycle, western flats being exposed two
hours earlier than the eastern ones. By gradually moving eastwards during low tide, birds can extend
their low tide feeding time to 16-17 hours.
Based on extensive research, van Gils et al. (2006) concludes that the presence of foraging knots on
the mudflats in the Wadden Sea matches most closely with an ideal, non-free model. ‘Non-free’ since
flights between foraging areas incur time and energy costs. ‘Ideal’, since knots appear to have good
information about the expected intake rate at each site. This may be necessary since prey densities
and hence, intake rates vary tremendously between sites, seasons and years (Zwarts, 1992). van Gils
et al. (2006) conclude that knots make state-dependent decisions by trading off starvation against
foraging-associated risks, including predation. Knots seem to share public information about resource
quality which enables them to behave in a more or less ideal manner.
The home range of individual knots in the Wadden Sea is large and amounts up to 800 km². With
respect to area use, van Gils et al. (2006) conclude that knots trade off energy intake rates against
travel cost. Thus, sites near a roost are skipped in case they offer low intake rates, while sites offering
high intake rates are only used if roosting occurs nearby. For example, Ballastplaat is more often used
by birds that roost at Griend (8-9 km away) than by Richel-roosters (16-18 km away). Knots wintering
in Scottish estuaries also show no or little site fidelity between years or within wintering seasons
(Symonds et al., 1984; Rehfisch et al., 2003), and roam over areas of several tens of square
kilometres in course of winter. By contrast, knots in Banc d’Arguin, Mauritania, were found to be very
faithful to their roosts, and used an area of only 2-16 km². This is in conformity with the behaviour of
birds wintering in tropic North-western Australia, where birds roam within an area of 20km² (Rogers et
al., 2006). The reason for this clear difference between tropical and temperate climate zones might be
that availability of prey is much more unpredictable in the temperate zones (Leyrer et al., 2006).
Prater (1972) found that stomachs of knots feeding by day contained four times the quantity of food
compared to the stomachs of night feeding birds. On the other hand, during premigration period,
(February-March) knots in Banc d’ Arguin seem to reach higher densities at night than during the day,
and Zwarts et al. (1990) found a night/day density ratio of 1,39. Sitters et al. (2000) reports night
foraging too, and also found a change in distribution during night time compared to daytime
distribution.
According to Lourenço et al. (2005), knots show strong association to intertidal drainage channels.
24
3.7 Sanderling (Calidris alba)
In literature, sanderling is often presented as typically occurring on sandy intertidal areas. In the
Wadden area they occur almost exclusively on sandy beaches and sand flats (Zwarts, 1981; van de
Kam et al., 1999); in the Delta area the majority of observations originate from sandy beaches (Wolff,
1969). In the Westerschelde, there exists a negative correlation between sanderling densities and the
silt content of the substrate (van Kleunen, 1999; Appendix I), and a comparable negative correlation
was found in the Tagus estuary by Granadeiro et al. (2004). In defining shorebird communities,
Granadeiro et al. (in press) found high densities of sanderling occurring on the coarser substrates,
coinciding with high densities of gulls. At the Orkneys, sanderlings, together with bar-tailed godwits
favour sandy sediments (Summers et al. 2002). Danufsky & Colwell (2003) found that substrate
particle size correlated positively with sanderling density in Humboldt Bay, California.
Some authors (van Turnhout & van Roomen, 2005) report a (small) difference in sediment preference
between Nearctic and Siberian populations. Sanderlings of the Nearctic population should have a
preference for muddier substrate compared to the Siberian birds. This is one of the reasons why some
authors (e.g. Engelmoer & Roselaar, 1998) plead for a division into two subspecies.
The sanderling shows a strong association with the tide line (De Meulenaer, 2006; Speybroeck et al.,
2006). Therefore one might expect sanderlings to be followers. However they behave in a very
opportunistic manner while feeding, and when food is abundant at emerged parts of the intertidal (eg.
concentration of wreck), sanderlings will readily gather there to form so-called feeding frenzies. This
way, sanderlings either behave as followers, or they behave in direct response to food abundance as
‘preferred area foragers’ (see Figure 2). According to van Kleunen (1999), sanderlings in the
Westerschelde occur throughout the intertidal area with a slight preference to areas with emersion
periods of 25-40% (Appendix I).
The species’ diet is very diverse and ranges from worms, over insects, to small amphipods and wreck
washed ashore. Scolelepis squamata is often mentioned as the most important food item for
sanderling (Dankers et al., 1983; De Gee, 1984; Glutz von Blotzheim et al., 1984). Recent research on
the Belgian coast however shows a rather marginal importance of Scolelepis squamata, and
sanderlings seem to depend largely on opportunistic feeding on wreck (all kinds of prey washed
ashore) (De Meulenaer, 2006; Speybroeck et al., 2006). Apparently, foraging on Scolelepis is
profitable only when the tide line crosses the narrow zone at the high intertidal where Scolelepis is
abundant. Whether this is due to deep burying of the worms in quickly drying sandy soils, or due to
high energy costs of probing in dry substrates is unclear.
25
26
3.8 Dunlin (Calidris alpina)
Dunlins show a clear preference for muddy substrates. Research in the Wadden Sea and the
Westerschelde estuary showed a positive correlation between dunlin densities and muddy sediments
(Ens et al., 1993; Brinkman & Ens, 1998; van Kleunen, 1999 (Appendix I); Ens et al., 2005). The data
of the Wadden Sea are visualised in Figure 10, and one sees that dunlins are encountered on a broad
range of sediment types, but reach highest densities on sediments with lutum content of 5-8%. In the
Tagus estuary in Portugal, Granadeiro et al. (2004 & in press) showed a positive correlation of dunlin
densities with the mud fraction of the soil. The same accounts for dunlins in the Wash (UK), where
densities are positively correlated with either the area of mud, or with the clay fraction (<20µm) of the
sediment, while a negative correlation was found with the sand fraction (>125µm) (Goss-Custard &
Yates, 1992; Yates et al., 1993). While investigating 494 coastal trajects on the Orkney islands (UK),
dunlins were found mostly on the muddy ones, together with Snipe, avocet, redshank and curlew
(Summers et al., 2002). On the other hand, Moreira (1999) found that the species’ habitat preference
in the Tagus estuary was not as explicit as reported by most, as dunlin took in an intermediate position
in a ranking of 13 species of waders according to their preference for sandy to muddy sediments.
Nehls & Tiedemann (1993) showed a seasonal pattern in habitat utilization and foraging-behaviour.
Generally, densities of dunlin were highest on muddy substrates, but in late summer, when there was
high availability of shrimps (Crangon crangon), dunlins preferred foraging on higher sandy sediments.
0,050
0,100
0,040
0,080
wader density (n/0,1ha)
wader density (n/0,1ha)
Some studies are conducted at a large special scale, and compare total numbers of wintering dunlin
between estuaries (McCulloch & Clark, 1992; Hill et al., 1993; Holloway et al., 1996). McCulloch &
Clark (1992) present a graph that shows the relationship between mean densities of dunlin and the
mean percentage of silt and clay in the sediments of 14 British estuaries (see Figure 11). Hill et al.
(1993) compared 109 British estuaries and identified four groups of estuaries with comparable wader
communities. The group containing the smaller and muddier estuaries was characterised by high
densities of dunlin, redshank and curlew. Finally, Holloway et al. (1996) and Austin et al. (1996)
related bird densities to estuary characteristics, and also found that dunlins are associated with the
more muddy estuaries.
0,030
0,020
0,010
0,060
0,040
0,020
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
lutum content (%)
Figure 10. Relation between densities of dunlin and the lutum content of the substrate (left) and emersion period
(right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002).
mean Dunlin density
birds/ha
20
15
10
5
0
0
20
40
60
80
100
m ean percentage silt+clay
Figure 11. The relationship between the mean proportion of silt and mud in the sediments of estuaries and the
densities of overwintering dunlin (birds/ha) (after McCulloch & Clark, 1992).
27
While in the Westerschelde van Kleunen (1999)(Appendix I) and Ens et al. (2005) found preference
for areas with long emersion periods, other studies show the opposite (Yates et al., 1993; Ens et al.,
1993; Brinkman & Ens, 1998; Granadeiro et al., 2006). In the Westerschelde, foraging dunlins possibly
make use of surface pools at the higher shoals (pers. comment Peter Meininger). Low tide water
counts in the Wadden Sea showed a clear preference for the lower parts of the intertidal (short
emersion times, see Figure 10). According to Granadeiro et al. (2006), dunlins behave like real tidefollowers, probably as a result of better prey availability (Esselink & Zwarts, 1989; Kelsey & Hassall
1989; Nehls & Tiedemann, 1993). Several authors stress on the importance of substrate penetrability
for tactile feeders like dunlin (Quammen, 1982 & 1984; Gerritsen & Van Heezik, 1985; Kelsey &
Hassal, 1989). For example, Kelsey & Hassal (1989) found that dunlins prefer low-lying wet areas with
high penetrability, even though density of the favoured prey was higher on the firmer ridges. Gerritsen
& Van Heezik (1985) showed that dunlins preferred to feed upon soft sediment rather than on firmer
substrate types, even if this choice reduced their foraging success.
Dunlin is said to be a typical worm-feeder, and the diet is dominated by oligochaetes and polychaetes
(mainly Nereis diversicolor). In case of high availability, the diet is added with Hydrobia ulvae, small
crustaceans (Crangon crangon, Corophium volutator) and small bivalves (Baltic tellin) (Wolff, 1969;
Cramp,1983; Kelsey & Hassall, 1989; Mouritsen & Jensen; 1992; Nehls & Tiedemann, 1993;
Mouritsen, 1994; Leopold et al., 2004).
According to Symonds et al. (1984) wintering dunlins are quite mobile within the estuary Firth of Forth
(Scotland), and they don’t seem to have great fidelity to high tide roosts. Dunlins even fly up to 18 km
between roosts and foraging areas. Rehfisch et al. (2003) also found poor fidelity to roosts, dunlin
being the third most mobile species out of eight in the Moray Basin, Scotland. These findings are in
contrast to what Dias et al. (2006a) report from the Tagus estuary. They found that dunlins only feed
close to their roost, and suggest that due to a lack of roosts, suitable foraging areas could remain
unexploited. According to studies conducted in the Wash estuary, adult dunlins also seem to be less
mobile (Minton, 1975; Cooper, 1988; Rehfisch et al., 1996) than reported from other estuaries in the
UK. However this is not the case in juvenile dunlins, as these are among the most mobile shorebirds
in the Wash. Rehfisch et al. (2003) offers an overview of several explanations for this age-related
difference. Juveniles may be more mobile in order to sample possible alternative future wintering sites.
Furthermore, juveniles may be forced to range more widely because of their lesser experience,
socially subordinate status, higher risk of being predated and possibly different diet.
Night foraging by dunlin is reported by several authors (e.g. Zwarts et al., 1990; Mouritsen, 1994;
Dodd & Colwell, 1996). Mouritsen (1994) reports that pecking is the dominant foraging technique by
day (interpreted as visual foraging), whereas probing was the preferred technique at night (tactile
foraging). They also tend to utilize different habitats during day and night time, with relatively more
birds aggregating on soft sediment containing high densities of Corophium volutator at night. When
tactile feeding, selected sites should indeed contain high densities of infaunal prey to maximize prey
encounter during probing. Soft sediment furthermore offers reduced costs and better prey accessibility
when probing. The results obtained by Mouritsen (1994) support the ‘supplementary hypothesis’
(shorebirds feeding at night only when daytime feeding has proved insufficient), however it does not
refute the ‘preference hypothesis’ (shorebirds feed at night because it is more profitable).
28
3.9 Bar-tailed godwit (Limosa lapponica)
Literature shows that bar-tailed godwits prefer intermediate to sandy environments. In the Wadden
Sea, Ens et al. (1993) found a positive correlation with the area of sandy sediments, and Brinkman &
Ens (1998) state that bar-tailed godwits avoid muddy areas, and prefer intermediate substrates. This
is visualised in Figure 12, showing that bar-tailed godwits occur on a broad range of sediments, but
clearly avoid sediments with lutum content of more than 8%. In the Westerschelde, the species was
found to avoid coarser substrates (van Kleunen, 1999)(Appendix I) requiring a silt content of at least
25%. According to Ens et al. (2005), bar-tailed godwits in the Westerschelde occur in a narrow range
of intermediate sediments. In the Wash (UK) the species shows positive correlation with the area of
sand (Goss-Custard & Yates, 1992), as well as with the content of fine sand (63-125µm) (Yates et al.,
1993). In the Orkneys too, the species prefers sandy areas (Summers et al., 2002). Hill et al. (1993)
defined four types of estuaries based on shorebird communities, and found that high densities of bartailed godwits generally occur in the broad and sandy estuaries (UK), and coincide with high densities
of knot, sanderling and oystercatcher. In western Africa, Guinea-Bissau, the bar-tailed godwit is placed
3rd in a ranking of 15 shorebird species according to their preference from sandy to muddy sediments
(Zwarts, 1988a). Moreira (1999) reports an intermediate sediment preference in the Tagus estuary. By
contrast, in defining four wader communities in the same estuary, Granadeiro et al. (in press) found
that highest densities of bar-tailed godwit coincide with high densities of dunlin, redshank and grey
plover, a community occurring on muddy sediments.
Foraging bar-tailed godwits are encountered on mussel beds too, and inland meadows can be
important as additional feeding grounds during winter and spring (Smit & Wolff, 1981; van de Kam et
al., 1999).
Bar-tailed godwits generally favour the low intertidal areas with short (Smith, 1975; Ens et al., 1993;
Tulp & de Goeij, 1994; Granadeiro et al., 2004) to intermediate emersion periods (Brinkman & Ens,
1998; van Kleunen, 1999 (Appendix I); Ens et al., 2005). Figure 12 shows clear avoidance of the
higher reaches of the intertidal area. The bar-tailed godwit is regarded as a follower by Thompson et
al. (1986), whereas it is classified as a non-follower by Granadeiro et al. (2006). This seems odd,
since the latter found a preference to areas with short emersion times during another study at the
same site (Granadeiro et al., 2004).
0,160
wader density (n/0,1ha)
wader density (n/0,1ha)
0,160
0,120
0,080
0,040
0,120
0,080
0,040
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
Figure 12. Relation between densities of bar-tailed godwits and the lutum content of the substrate (left) and
emersion period (right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert,
2002).
In the Westerschelde, Ruiters (1992) studied faeces of bar-tailed godwits. He found that worms
(Nereis and others) form the staple food, added with few bivalves (mussel, cockle, Baltic tellin) and
Hydrobia. When temperature drops beneath 3°C intake rate of Arenicola decreases, and bar-tailed
godwits switch to Scoloplos and Notomastus, which were found by the sewing technique, and thus
most probably by tactile means (Smith, 1975). The species’ diet is diverse however, and recent
research in the German Wadden Sea showed a total of 17 prey species, the most important items still
being worms (Nereis, Nephtys and Scoloplos). In autumn Arenicola marina seems very important, and
comprises 24% in the male’s and 65% in the female’s prey mass (Scheiffarth, 2001). According to
Smith (1975), bar-tailed godwits follow the tide edge closely, on both ebb and flood, for the numbers of
29
their prey (Arenicola marina) visible at the surface declines steadily after the tide has passed. Smith
(1975) also found that the godwits found more Arenicola in wet sediments, and therefore avoid sandy
areas that dry out during low tide. Lourenço et al. (2005) reports a strong association with drainage
channels (where sediments also remain wet), probably due to exceptionally high densities of Nereis
diversicolor near these channels (pers. comm. Pedro Lourenço).
Night foraging has been reported by Zwarts et al. (1990) and Ntiamoa-baidu et al. (1998). During
premigration period in Banc d’ Arguin, Mauritania, bar-tailed godwits reach highest densities during
night time, with a night/day density ratio of 1,22 (Zwarts et al., 1990).
Both et al. (2003) report a different use of the tidal flats by males compared to females, as a result of
sexual dimorphism (males having shorter bills). Males were concentrated on exposed mud flats, while
females occurred more along the waterline. According to Both et al. (2003) also, the waterline seems
to be a better foraging habitat for bar-tailed godwits, since intake rates are higher there. Females thus
seem to monopolise the better quality foraging areas, since males were more susceptible to
intraspecific kleptoparsitism.
Bar-tailed godwits are mobile birds, and show poor fidelity to high tide roosts, as shown by research in
the Firth of Forth and the Moray basin, Scotland (Symonds et al., 1984; Rehfisch, 2003).
30
3.10 Curlew (Numenius arquata)
In general, densities of curlew show a positive correlation with muddy substrates. This is found by
research conducted in Guinea-Bissau (Zwarts, 1988a), in the Wash (UK) (Goss-Custard & Yates,
1992; Yates et al., 1993), on the Orkney islands (UK) (Summers et al., 2002), in the Westerschelde
(van Kleunen, 1999 (Appendix I); Ens et al., 2005) and in the Wadden Sea (Ens et al., 1993). Only
Brinkman & Ens (1998) report that the favoured habitat in the Wadden Sea consists of intermediate to
muddy sediment. The results of low tide counts in the Wadden Sea indeed show that foraging curlews
can be found at a broad range of sediment types with a preference for intermediate substrates (lutum
content 3-5%). When distinguishing shorebird communities, Hill et al. (1993) found that high densities
of curlew occur in the more muddy estuaries, and coincide with high densities of dunlin, redshank and
avocet. Furthermore, curlews may show a strong association with mussel beds (Smit & Wolff, 1981;
Ens et al., 1993).
There is poor agreement in literature about the tidal behaviour of curlews. Several authors report
curlews are followers (Thompson et al., 1986), or favour the low intertidal (Yates et al., 1993;
Brinkman & Ens, 1998; van Kleunen, 1999). Looking at Figure 13 it seems that curlews in the Wadden
Sea avoid the highest intertidal areas, and show a preference for relatively short to intermediate
emersion times of 4 to 5,5 hours. In the Westerschelde estuary, van Kleunen (1999) found curlews
occurring throughout the intertidal range with a preference for emersion periods less than 40%. This is
in contrast to what Ens et al. (2005) found in the Westerschelde, namely curlews preferring areas with
rather long emersion periods. Tulp & de Goeij (1994) state that in contrast to the real followers,
Eastern curlews in Roebuck Bay, North-western Australia, also use parts of the intertidal that are
already exposed for longer periods. Some authors state that curlews are non-followers (Recher, 1966;
Townshend et al., 1984 in: Danufsky & Colwell, 2003).
0,400
wader density (n/0,1ha)
wader density (n/0,1ha)
0,400
0,300
0,200
0,100
0,300
0,200
0,100
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
Figure 13. Relation between densities of curlew and the lutum content of the substrate (left) and emersion period
(right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002).
Based on an extensive literature review, Leopold et al. (2004) concludes that the diet of curlews is
very diverse, consisting mainly out of bivalves and large worms (Nereis and Arenicola), added with
20% other prey such as Carcinus maenas and shrimps. Small prey like little worms or Hydrobia ulvae
are unimportant to the large curlew. In the Westerschelde, most important prey items are Nereis,
followed by Carcinus maenas and bivalves (Ens et al., 2005). Curlews aren’t strictly bound to intertidal
flats and are often seen on inland meadows where they forage on earthworms (Lumbricus terrestris)
and other typical inland prey (Diptera-larvae). Some curlews spend the whole winter inland, others
only during severe weather or high tides (van de Kam et al. 1999).
Thomspon et al. (1986) showed a negative correlation between curlew and densities of Nereis. This is
in fact not a contradiction since the largest (and most profitable) Nereis were rare where overall Nereis
density was high. According to Zwarts (1996b), curlews select prey of the most profitable sizes. For
example, amongst the prey caught by curlew, Nereis of 12 cm occurred 5 times more often than
Nereis of 6 cm. Taking prey densities and accessibility (burying depth varies with worm length) into
account this means that Nereis of 12 cm are selected 23 times more often. Similarly, curlews preferred
Mya arenaria of 4-5 cm. In the case of Carcinus maenas, individuals smaller than 10mm are ignored.
31
Zwarts & Esselink (1989) report two different methods that curlew use to capture Nereis diversicolor.
They search for worms at the surface which are taken with a single peck, or they search for visual
cues such as burrow entrances or traces (water current) due to filter feeding activity, and probe deep
to extract the worm from the burrow. Nereis taking through probing is common in summer, but this
behaviour disappears in autumn due to a decreased accessibility (increase of burrowing depth and a
reduction of the filter feeding). Foraging behaviour of curlews is strongly influenced by the behaviour of
its prey. Worms cannot filter-feed on dry surfaces and thus filter-feeding is generally restricted to the
first 2 hours after exposure of the intertidal area. Afterwards worms must surface to graze. In other
words: during the low water period filter activity decreases, while grazing activity increases, resulting in
a shift between foraging modes of curlew. Nereis activity is also influenced by the sediment type.
Generally, in muddy soils, Nereis will tend to graze more often, since silt particles interfere with
filtering activities. Also, filtering is less profitable when the water contains few food particles as at the
end of winter, so grazing will then be more efficient (Esselink & Zwarts, 1989).
The sexual dimorphism in curlews may result in a segregation in habitat choice (Townshend, 1981),
as well as in diet choice (Zwarts & Wanink, 1984). In the Tees estuary (North-east England), relatively
more males compared to females feed on adjacent fields during winter. Townshend (1981) suggest
this is due to the deep burying of Nereis as temperatures drop and Nereis becomes more and more
unavailable to the short-billed male curlews. Zwarts & Wanink (1984) state that in the Wadden Sea,
male curlews take few Mya arenaria only, while it is a main prey item of females. These authors
suggest that the accessible proportion of Mya arenaria above the lower size limit is too small for the
shorter-billed males.
Curlews prefer feeding during the day, but may also feed at night when daytime food intake becomes
insufficient (Cremer & Hupkes, 1984, in: van de Kam et al., 1999). The foraging activity of curlews that
were followed from July until November increased from 65% to 80%, however, this did not
compensate for the decreasing foraging time available. In the meanwhile, night time foraging
increased, from ½ hour to nearly 5,5 hours. Thus, birds in November foraged 1,5 times as long as
birds in July, but overall intake rate stayed nearly the same throughout the period, as night time
foraging success was 30% lower compared to day time foraging success. During premigration period
in Guinea-Bissau (February-March), Zwarts et al. (1990) found a ratio of night to day foraging numbers
of 0,58. Ntiamoa-baidu et al. (1998) also report curlews feeding by night.
In Scotland, curlews show high fidelity to high tide roosts as reported by Rehfisch et al. (2003).
Through colour ring marking of several hundreds of curlew in the Wadden Sea, high (foraging) site
fidelity could be shown. Marked birds seemed to forage at exactly the same sites for years in a row,
some defending an area as small as 0,2 to 1 ha. If in particular years, there was not enough food
within their own territory, the birds often kept foraging within 1 km of that site (Ens & Zwarts, 1980;
Cremer & Hupkes, 1984; in: van de Kam et al., 1999).
32
3.11 Spotted redshank (Tringa erythropus)
According to Blomert (2002), the spotted redshank prefers muddy sediments, and Smit & Wolff (1981)
also describe the preferred habitat in the Wadden Sea as very muddy shallows. By contrast, Brinkman
& Ens (1998) mention spotted redshank as a bird of intermediate substrates. Low tide counts in the
Wadden Sea revealed a strong preference to soils with a lutum content of 5-8%, and an exposure
period of 7 hours (Figure 14). Feeding generally takes place in shallow water, and foraging birds are
often encountered in the creeks of saltmarshes or in ditches in inland polders. Foraging birds usually
walk in the water and sometimes even swim (van de Kam et al., 1999).
In tidal areas they search for Nereis, Carcinus maenas, shrimps and smaller prey like Corophium
volutator. In summer spotted redshanks also hunt for young fish and shrimps trapped in pools (van de
Kam et al., 1999; Leopold et al., 2004). The bird sometimes uses side-to-side scything movements like
avocet, with bill inclined at shallow angle to surface (Cramp, 1983).
0,020
0,020
0,016
0,016
wader density (n/0,1ha)
wader density (n/0,1ha)
Just like avocet, Ntiamoa-baidu et al. (1998) classify spotted redshank as a pelagic forager. This type
of wader hunts for fish in the water layer, and uses visual as well as tactile senses to detect prey.
When foraging on fish or shrimps, social feeding is often seen, not seldom in association with avocets
(Ntiamoa-baidu et al., 1998; van de Kam et al., 1999). Ntiamoa-baidu et al. (1998) reports night
foraging.
0,012
0,008
0,004
0,012
0,008
0,004
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
Figure 14. Relation between densities of spotted redshank and the lutum content of the substrate (left) and
emersion period (right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert,
2002).
33
34
3.12 Redshank (Tringa totanus)
Redshanks generally prefer muddy sediments, although some authors found a preference to
intermediate substrates. Brinkman & Ens (1998), for example, report a preference to intermediate
sediments in the Wadden Sea. Ens et al. (1993), however, found positive correlations with the low
muddy areas (most significant), as well as with the low sandy areas, as with the area of mussel bed.
Looking at Figure 15, redshanks in the Wadden Sea show a clear avoidance of the coarse sediments
and reach peak densities at areas with a fairly high lutum content of 5-8%. In the Westerschelde,
redshanks clearly prefer the muddy areas (van Kleunen, 1999 (Appendix I); Ens et al., 2005). In
Guinea-Bissau, Zwarts (1988) found well defined peak densities at muddy sand, and redshank took in
an intermediate position in a ranking according to the species’ preference from sandy to muddy
substrate. In the UK, results of research show good agreement. In the Wash, densities of redshank
show a positive correlation with the area of mud, as well as with the clay content (<20µm) of the
substrate, and moreover, densities show a negative correlation to the sand content (>125µm) (Gosscustard & Yates, 1992; Yates et al., 1993). Hill et al. (1993) compared wader communities in 109
British estuaries, and distinguished four types of estuaries. The smaller, more muddy estuaries held
highest densities of redshank, together with dunlin, curlew and avocet. At the Orkney islands,
redshanks occur on muddy substrates, and are associated with snipe, curlew, dunlin and avocet
(Summers et al., 2002).
0,500
0,500
0,400
0,400
wader density (n/0,1ha)
wader density (n/0,1ha)
The redshank’s diet is diverse, comprising of several species of worms (Nereis, Nephtys, Lanice,
Scoloplos, Harmothoe), Crustacea (small crabs as well as shrimps and Corophium) and Hydrobia (see
literature review by Leopold et al., 2004). Inland meadows can provide an alternative and additional
food source (van de Kam et al., 1999).
0,300
0,200
0,100
0,300
0,200
0,100
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
Figure 15. Relation between densities of redshank and the lutum content of the substrate (left) and emersion
period (right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002).
According to van Kleunen (1999) there is a negative correlation between redshank densities and the
emersion period (Appendix I). Yates et al. (1993) and Ens et al. (1993) both found a positive
correlation between densities of redshank and area of low lying mud, respectively in the Wash (UK)
and the Wadden Sea. Goss-custard & Yates (1992) report that redshanks are mainly associated with
creeks and the tide edge. Likewise, Granadeiro et al. (2004) report a negative correlation between
redshank densities and exposure period in the Tagus estuary, while Lourenço et al. (2005) reports a
strong association with drainage channels. On the other hand, Granadeiro et al. (2006) states
redshank being a non-follower. Furthermore, research in the Netherlands showed that the species
occurs on habitats with a wide range of emersion periods (Brinkman & Ens, 1998), in the
Westerschelde even favouring areas with long emersion times according to Ens et al. (2005), in
contrast to van Kleunen (1999). According to the low tide count in the Wadden Sea as shown in Figure
15, redshank occur on a broad range of exposure periods, but clearly avoid areas with long emersion
times.
The amphipod Corophium is often mentioned as a favoured prey species (Goss-Custard, 1969 &
1977b). When preying on Corophium, the habitat preferences and tidal and seasonal variation in
activity and availability of this benthic prey species greatly determines the foraging behaviour of
redshanks. For example, when temperature drops beneath 6°C, Corophium becomes less active and
35
the birds take increasing numbers of Baltic tellin or Nereis diversicolor (Goss-Custard, 1969). On a
tidal scale, when receding tide has just exposed the flats, Corophium is very active. Their activity then
steadily decreases, thus redshanks follow the retreating tide line to maximize intake rate. This
suggests that redshank are so-called followers, favouring the low tidal flats (Zwarts, 1974; Thompson
et al., 1986; van de Kam et al., 1999). Boates (1980) found that on the receding tide line large sized
adults of Corophium are active. This is a short-lived phenomenon however, and within half an hour of
the tide passing, only 5% of the initial number of Corophium is active on the surface.
Redshanks foraging on Nereis obey the optimal foraging theory and select larger prey in respect to
their profitability. The preferred size classes of worms had the highest ratio of energy content to
handling time, as predicted by the optimal foraging theory. On the other hand, redshanks feeding on
Corophium did not seem to actively select larger prey. When larger Corophium were taken, this
appeared to reflect the greater chance of large individuals being detected as large Corophium provide
larger visual clues (Goss-Custard, 1977).
Several authors report nocturnal foraging by redshank (Goss-Custard, 1969; Zwarts et al., 1990;
Ntiamoa-baidu et al., 1998; van de Kam et al., 1999; Burton & Armitage, 2005). Normally redshanks in
the Ythan (UK) pecked at the mud surface for Corophium, but swished their bills from side to side in
darkness and ate gastropods (Goss-Custard, 1969). Burton & Armitage (2005) found that at night,
redshanks in the Severn estuary use different foraging areas than during the day. Notwithstanding the
fact that the site visited at night held very high densities of Corophium, this is probably explained by
the presence of a heliport causing disturbance during the day. Zwarts et al. (1990) found a ratio of
night/day densities of 0,39 in Banc d’ Arguin, Mauritania.
In Scotland, redshanks are not very mobile and show high fidelity to their roosts (Symonds et al.,
1984; Rehfisch et al., 2003).
36
3.13 Turnstone (Arenaria interpres)
Turnstones show a strong association with hard substrates (rocky shores but also all kinds of human
constructions like groynes, dykes etc.). However, as a highly opportunistic species it is also found at
various types of tidal flats (sand as well as mud) and along the tide line, where it feeds on all kinds of
prey washed ashore (Smit & Wolff, 1981; Cramp, 1983; van de Kam et al., 1999; Engledow et al.,
2001; Summers et al., 2002; Becuwe et al., 2006; Speybroeck et al., 2006). The small numbers of
turnstones present in the Wadden Sea seem to prefer the more sandy substrates (see Figure 16). A
preference for sandy substrate in the Wadden Sea was also found by Ens et al. (1993). In GuineaBissau however, turnstones reach peak densities on muddy sands and take in 11th position in a
ranking of 15 shorebird species according to their preference from sandy to muddy substrates (Zwarts,
1988a). In the Westerschelde, van Kleunen (1999) encountered highest density of turnstones on
muddy sediments with silt content of more than 50% (Appendix I). Along the Belgian coast, turnstones
may also show a preference for muddy areas, especially during summertime, for example in the IJzer
estuary and the harbour of Zeebrugge. During high tides in winter, foraging turnstones can also be
found in meadows and fields in the polder land (Becuwe et al., 2006).
The name of the species refers to their unique behaviour of turning stones, shells or other items; once
the item is turned over, all kind of prey may come available (Cramp, 1983; van de Kam et al., 1999).
Their strong, stout bill can also be used to break open shells and crabs, and to peck barnacles from
rocks. According to Becuwe et al. (2006) their diet along the Belgian coast diet is very diverse and
prey taken ranges from Crustaceans (crabs, Gammarus) and Barnacles, over worms (Nereis, Eulalia)
and insects to mussels and even bread thrown by humans. Leopold et al. (2004) state that turnstones
probably take anything that is eatable, and the number of invertebrate species taken as food varies
enormously, depending on place and time of the year. In the Westerschelde, Ruiters (1992) found
shellfish (Baltic tellin, Hydrobia; most probably eaten as wreck), Nereis, Corophium and insects as
main prey items.
Turnstones foraging on beaches often occur along the tide line, searching for food washed ashore.
However, being highly opportunistic, they respond quickly to local food abundance, and readily exploit
emerged parts of the intertidal when food in the form of wreck is abundant (Speybroeck et al., 2006).
Turnstones in North-western Australia were also observed foraging along the tide line as well as on
parts already exposed for a longer period (Tulp & de Goeij, 1994). In the Wadden Sea, Ens et al.
(1993) found a positive correlation with the area of low intertidal sand flats. Based on the low tide
counts in the Wadden Sea (Figure 16), one sees two very distinct peak densities, one at intermediate
emersion time (5,5h), and one at very short emersion time (3h). Because of very low densities
encountered, these results may be unreliable. In the Westerschelde, turnstones are most often
encountered on areas with rather short emersion periods of less than 40% (van Kleunen, 1999;
Appendix I).
0,016
wader density (n/0,1ha)
wader density (n/0,1ha)
0,004
0,003
0,002
0,001
0,012
0,008
0,004
0,000
0,000
<0.5
.5-1.5 1.5-3.0
3-5
5-8
lutum content (%)
8-12
12-18
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
7.0
7.5
emersion period (hours)
Figure 16. Relation between densities of turnstone and the lutum content of the substrate (left) and emersion
period (right), based on low tide counts in the Wadden Sea (after Zwarts, unpublished data, in: Blomert, 2002).
Since turnstones largely depend on visual information while foraging they are exclusively day-active
in a day-night rhythm. During the day, turnstones show a tidal rhythm; they forage around low tide and
37
aggregate in roosts at high tide (Becuwe et al., 2006). Other studies confirm their diurnal foraging
pattern, like for example in the Banc d’ Arguin, Mauritania (Zwarts et al., 1990) and in Ghana
(Ntiamoa-baidu et al., 1998).
In the UK, turnstones show a high degree of site fidelity to foraging grounds as well as to high water
roosts (Symonds et al., 1984; Rehfisch et al., 2003).
38
4 EXPERT INQUIRY
4.1 Introduction
Five out of twenty contacted shorebird experts were prepared to fill in our inquiry form. These were
Bruno Ens (SOVON, the Netherlands), Pedro Lourenço (Universidade de Lisboa, Portugal), Peter
Meininger (RIKZ, the Netherlands), Geert Spanoghe (INBO, Belgium) and Michael Yates (Centre for
Ecology and Hydrology, United Kingdom). Please note that the order of experts as listed in the
previous sentence is alphabetically and does not correspond to the numerical order as given in the
tables below.
The first question in this inquiry dealt with sediment preference of waders. The experts were asked:
•
•
•
to classify the waders according to their habitat preference from muddy to sandy substrates
(ranking),
to generally describe the preferred habitat using the terms sandy, intermediate and muddy
and
to score the dependence of the wader on the preferred sediment type.
In the second question the experts were asked to classify the wader species according to their tidal
preferences (from low to high intertidal areas), and to point out which species are followers and which
are non-followers.
The third question was established to learn more about the dependency of the birds to one or more
prey species, the most important prey species and the habitat demands of the prey species.
Finally, the experts were asked to sum up any other factors that might be of significance for the
distribution of waders, and to ventilate remarks concerning our investigation.
In Appendix III one can find the original question form.
4.2 Sediment
There is good agreement among the experts about the habitat preferences of avocet, sanderling,
dunlin and redshank Table 1. By contrast, for knot, bar-tailed godwit and grey plover there is poor
agreement concerning their habitat preference.
Table 1. Results of the inquiry for the sediment preference, including a ranking of the birds according to their
sediment preference (1 = occurring on most sandy sediments … 13 = occurring on most muddy sediments), and
a classification of the favoured sediment (M = muddy, I = intermediate, S = sandy).
EXPERT 1
EXPERT 2
EXPERT 3
EXPERT 4
EXPERT 5
oystercatcher
2
S
6
6
I
4
S
4
I
avocet
13
M
13
12
M
13
M
13
M
ringed plover
6
I
5
3
S
3
S
7
I
Kentish plover
5
I
1
1
S
2
S
grey plover
9
I
11
4
S
4
I
6
M
knot
4
I
4
8
I
5
I
11
M
sanderling
1
S
2
2
S
1
S
1
S
dunlin
10
I
10
7
I
7
I
10
M
bar-tailed godwit
8
I
3
10
M
2
S
12
M
curlew
7
I
8
9
I
7
I
5
I
spotted redshank
11
M
12
13
M
10
M
8
M
redshank
12
M
9
11
M
10
M
9
M
turnstone
3
I
7
5
I
8
I
3
S
39
For each species we calculated an average ranking based on the expert rankings (Table 2). Next, a
mean number was calculated based on the experts’ classifications of the preferred habitat, which was
consequently converted to one of four following categories: sandy = <1,5; muddy sand = 1,5-2; sandy
mud = 2-2,5; muddy = >3). The same was done for the dependency of the waders to their favoured
habitat (high specifity= 1-1,7; intermediate specifity= 1,7-2,3; poor specifity= 2,3-3).
Table 2. Mean ranking according to habitat preference of waders based on expert judgement; classification of
preferred habitat in 4 categories (sandy, muddy sand, sandy mud, mud). The degree of dependency on the
sediment is expressed by the colour (yellow=high specifity; green=intermediate specifity; orange= low specifity).
Avg.
Class
Specifity
Species
Preferred sediment
Ranking
sanderling
Sandy
1,4
1
1
Kentish plover
Sandy
2,3
1,333
1,5
oystercatcher
Intermediate (muddy sand)
4,4
1,5
2,2
ringed plover
Intermediate (muddy sand)
4,8
1,5
2
turnstone
Intermediate (muddy sand)
5,2
1,75
2,6
knot
Intermediate (sandy mud)
6,4
2,25
1,8
grey plover
Intermediate (sandy mud)
6,8
2
2
bar-tailed godwit
Intermediate (sandy mud)
7,0
2,25
1,8
curlew
Intermediate (sandy mud)
7,2
2
2,6
dunlin
Intermediate (sandy mud)
8,8
2,25
2,2
redshank
Muddy
10,2
3
2,2
spotted redshank
Muddy
10,8
3
1,6
avocet
Muddy
12,8
3
1,2
Based on these results we can conclude that sanderling and Kentish plover strongly depend on sandy
sediments. Moreover, expert judgement shows that they are strongly bound to this sediment type
(Table 2). A similar strong preference, but for muddy substrate, was suggested for spotted redshank
and avocet. According to the experts, all other wader species exhibit a less strong habitat preference,
with turnstone and curlew exhibiting the lowest habitat preference. Oystercatcher is third in row, and
this matches well the general findings in literature that this species is found in highest densities on
rather sandy soils. Ringed plover, turnstone, knot occur on intermediate substrates with a slight
preference for the sandy ones. Grey plover, bar-tailed godwit, curlew and dunlin are also mainly found
on intermediate substrates, but show a preference for the more muddy substrates. Redshank, spotted
redshank and avocet end up at the other extreme of the ranking.
In general, these results are quite consistent with what could be deducted from literature. The result
for Kentish plover however is in contrast to what was found in the very few literature reporting on
habitat preference by this species (preference to muddy substrates). Again it appears that knowledge
on habitat preference by Kentish plover is largely unavailable.
40
4.3 Emersion time
There is very poor agreement among experts in the results of the inquiry question dealing with
emersion time preference (Table 3). Possibly, the disagreement reflects large variability of foraging
behaviour of shorebirds, both in time and in space. Therefore, in situ results obtained by van Kleunen
(1999) and Ens et al. (2005) are probably of much more value.
Table 3. Results of the inquiry for emersion time preference, including a ranking of the birds according to their
habitat preference (1 = occurring on lowest parts of the intertidal … 13 = occurring on the highest parts), and a
classification of the birds according to their tidal behaviour (follower/non-follower).
EXPERT 1
EXPERT 2
EXPERT 3
EXPERT 4
EXPERT 5
oystercatcher
2
FO
11
NF
7
NF
4
NF
10
NF
avocet
12
NF
1
FO
6
FO
10
NF
1
FO
ringed plover
5
NF
7
NF
11
NF
12
NF
8
?
Kentish plover
13
NF
8
NF
13
NF
?
?
11
?
grey plover
10
FO
6
NF
12
NF
6
NF
6
NF
knot
4
FO
9
NF
3
NF
8
NF
3
FO
sanderling
8
FO
12
NF
10
FO
1
FO
12
FO
dunlin
1
FO
10
NF
2
NF
10
FO
2
FO
bar-tailed godwit
11
FO
5
FO
1
FO
6
NF
7
NF
curlew
3
FO
4
FO
8
NF
4
NF
9
?
spotted redshank
9
FO
3
FO
4
FO
2
?
4
?
redshank
7
FO
2
FO
5
NF
12
FO
5
NF
turnstone
6
NF
13
NF
9
FO
6
FO
13
?
Table 4 shows the average ranking according to the preference of the waders going from low to high
intertidal flats. Since there is poor consistence between the results obtained, one may doubt the value
of this ranking. In the column ‘agreement among experts’ the difference between minimum and
maximum ranking values given by the experts is shown (as presented in Table 4).
In the case of tidal behaviour (follower/non-follower), the result is shown in bold when there is good
agreement among experts.
Table 4. Mean ranking according preference from lowest to highest intertidal areas, based on expert judgement,
and classification of tidal behaviour.
Agreement
Mean
Species
Tidal behaviour
among
ranking
experts
spotted redshank
follower
4,4
7
dunlin
?
5,0
9
knot
?
5,4
6
curlew
?
5,6
6
avocet
?
6,0
11
bar-tailed godwit
?
6,0
10
redshank
?
6,2
10
oystercatcher
non-follower
6,8
9
grey plover
non-follower
8,0
6
ringed plover
non-follower
8,6
7
sanderling
follower
8,6
11
turnstone
?
9,4
7
Kentish plover
non-follower
11,3
5
Spotted redshank and sanderling are regarded as typical followers, whereas oystercatcher, grey,
ringed and Kentish plover should behave like non-followers. In literature too, plovers are generally
regarded as non-followers. A contradictory result was obtained for sanderling. While this species is
41
regarded as a follower by four out of five experts, it ends third last in the ranking, suggesting
sanderling mainly occurs on the higher intertidal areas. Personal comment obtained by two of the
experts did not result in a satisfactory explanation for this contradiction.
4.4 Food choice
When looking at Table 5, one sees that avocet, bar-tailed godwit, and especially knot and
oystercatcher are highly specialised feeders, depending on a limited range of prey species. It seems
obvious that these specialised species will suffer more of changes in their environment than
opportunistic feeders like turnstone or sanderling would do. These results are consistent with what
was found in literature.
Table 5. Results of the inquiry: food specialisation and diet of shorebird species (yellow = highly specialised;
green = moderately specialised; orange = non-specialised, opportunistic). The order of the bird species is
according to their food specialisation; in the second column, the order of the prey species is according to their
importance.
Species
Prey items
turnstone
diverse, bivalves, crustaceans, polychaetes
sanderling
crustaceans (!), worms, polychaetes, insects
Kentish plover
worms, insects, crustaceans
dunlin
worms (!), polychaetes, crustaceans
curlew
Carcinus maenas, worms, Nereis, Arenicola, Mya arenaria, insects, crustaceans
spotted redshank
crustaceans, polychaetes, fish
redshank
crustaceans, Corophium, Nereis, Hydrobia, polychaetes
ringed plover
worms, polychaetes, insects, crustaceans
grey plover
worms, Arenicola, polychaetes, insects, crustaceans
avocet
(small) Nereis, Hydrobia, worms, insects, crustaceans
bar-tailed godwit
worms (!), Arenicola, polychaetes
knot
cockle, Baltic tellin, other (small) bivalves
oystercatcher
cockle (!!), mussel, Baltic tellin
42
5 RECOMMENDATIONS
This literature study shows that there is quite good agreement concerning sediment preference by
waders. Moreover, the results obtained by the inquiry are consistent to what is found in literature.
The opposite is true for tidal foraging behaviour and emersion period preference. Literature as well as
the results of the inquiry show very poor agreement, which makes it difficult to make definite
statements. As far as we can judge, tidal behaviour and emersion period preference seems to vary
seasonally (in accordance to variation in food availability) and varies among estuaries. However, good
knowledge on this subject is essential to correctly predict shorebird distribution.
Lourenço et al. (2005) showed the importance of the small-scale effect of drainage channels on
shorebird densities. However, little was found on the importance of other small-scale features that
characterise intertidal areas, such as mussel beds and surface pooling. Mussel beds, however, are
encountered at only two locations in the Westerschelde. Surface pooling in particular might be very
important in determining shorebird distribution, as it affects tidal behaviour, and may even influence
sediment preference (pers. comment Peter Meininger & Bruno Ens).
To assess emersion period preference by shorebirds, and to evaluate the influence of small-scale
intertidal features on shorebird distribution, we advise further study. This study should be conducted in
the Westerschelde itself, if possible throughout the whole year, in order to detect seasonal variation.
To fully understand habitat preference of waders in the Westerschelde the study should cover the full
tidal cycle.
43
44
REFERENCES
Austin, G., Rehfisch, M.M., Holloway, S.J., Clarck, N.A., Balmer, D.E., Yates, M.G., Clarke, R.T.,
Swetnam, R.D., Eastwood, J.A., Durell, S.E.A. le V dit, West, J.R. Goss-Custard, J.D. (1996).
Estuaries, Sediments & Shorebirds III: Predicting Waterfowl Densities on intertidal Areas. BTOresearch-Report (ETSU T/04/00207/REP) ETSU, Harwell.
Atkinson, P.A., Crooks, S., Drewitt, A., Grant, A., Rehfisch, M.M., Sharpe, J. & Tyas, C.J. (2004).
Managed realignments in the UK-the first 5 years of colonization by birds. Ibis 146: 101-110.
Becuwe, M., Lingier, P., Deman, R., De Putter, G., Devos, K., Rappé, G. & Sys, P. (2006).
Ecologische atlas van de Paarse strandloper en de Steenloper aan de Vlaamse kust 1947-2005. VLIZ,
Oostende. 184p.
Beukema, J.J., Essink, K., Machielis, H. & Zwarts, L. (1993). Year-to-year variability in the biomass of
macrobenthic animals on tidal flats of the Wadden Sea: how predictable is this food source for birds?
Neth. J. Sea Res. 13: 331-353.
Blomert, A.M. (2002). De samenhang tussen bodemgesteldheid, droogligtijd en foerageerdichtheid
van vogels binnen de intergetijdenzone, A&W-rapport 330, Altenburg & Wymenga ecologisch
onderzoek, Veenwouden.
Boates, J.S. (1980). Foraging Semipalmated sandpipers Calidris posilla L. and their major prey
Corophium volutator on the Starrs Point mudflat Minas Basin, Unpublished M.S. thesis, Acadia
University, Canada.
Boettcher, R. & Haig, S.M. (1995). Habitat-related factors affecting the distribution of non-breeding
American avocets in coastal South Carolinia. The Condor 97:68-81
Both, C., Edelaar, P. & Renema, W. (2003). Interference between the sexes in foraging bar-tailed
godwits Limosa laponica. Ardea 91(2): 268-272.
Brinkman, A.G. & Ens, B.J. (1998). Effecten van bodemdaling in de Waddenzee op wadvogels. IBNrapport 371, Wageningen.
Brinkman, A.G., Meesters, E.H.W.G., Dijkman, E.M. Brenninkmeijer, A., Kersten, M, Ens, B.J. (2005).
Habitatgebruik van foeragerende wadvogels in de Westerschelde. Datarapport RKZ 1267, AlterraTexel, Altenburg & Wymenga.
Bryant, D.M. (1979). Effects of prey density and site character on estuary usage by overwintering
waders (Charadrii). Estuarine and Coastal Marine Science 9: 369-384.
Burger, J. & Olla, B.L. (eds.) (1984). Shorebirds. Migration and foraging behaviour. Plenum Press,
New York and London, 329p.
Burton, N.H.K. & Armitage, M.J.S. (2005). Differences in the diurnal and nocturnal use of intertidal
feeding grounds by redshank Tringa totanus: Capsule redshank used more sites and had larger
ranges at night than during the day. Bird Study 52(2): 120-128.
Burton, N.H.K., Musgrove, A.J. & Rehfisch, M.M. (2004). Tidal variation in numbers of waterbirds: how
frequently should birds be counted to detect change and do low tide counts provide a realistic
average? Bird Study 51: 48-57.
Chapman, M.A.G. (1949). The thixotropy and dilatancy of marine soil. J. Mar. Biol. Ass. U.K. 28: 123140.
Clark, N.A. (2006). Tidal barrages and birds. Ibis 148: 152-157.
45
Colwell, M.A. & Landrum, S.L. (1993). Non-random shorebirds distribution and fine-scale variation in
prey abundance. The Condor 95: 94-103.
Cooper, R.H.W. (1988). Migration strategies of shorebirds during the non-breeding season with
particular reference to the sanderling (Calidris alba). PhD-thesis University of Durham, Durham.
Cramp, S. & Simmons, K.E.L. (eds.) (1983). Handbook of the birds of Europe, the middle east, and
North Africa: the birds of the western Palaearctic. Vol. 3: waders-gulls. Oxford University, Oxford.
913p.
Cresswell, W. (1994a). Age-depending choice of redshank (Tringa totanus) feeding location:
profitability or risk? Journal of Ecology 63: 589-600.
Cresswell, W. (1994b). Flocking is an effective anti-predation strategy in redshanks (Tringa totanus).
Animal Behaviour 47: 433-442.
Cremer, J. & Hupkes, R. (1984). Voedselterritoria bij de wulp: lange en korte termijn voordeel.
Studentenrapport, Zoölogisch laboratorium Rijksuniversiteit Grongingen / Rijksdienst voor de
IJsselmeerpolders, Lelystad.
Dankers, N., Binsbergen, M. & Zegers, K. (1983). De effecten van zandsuppletie op de fauna van het
strand van Texel en Ameland. RIN-rapport 83/6, Rijksinstituut voor Natuurbeheer, Texel.
Danufksy, T. & Colwell, M.A. (2003). Winter shorebirds communities and tidal flat characteristics at
Humbolt bay, California. The Condor 105: 117-129.
Darby, J. (1975). Dispersion pattens of the lugworm Arenicola marina. Unpublished Hons. Thesis,
Department of Zoology, University of Edinburgh.
De Gee, T. (1984). Een onderzoek naar de verspreiding en populatiedynamica van Scolelepis
squamata op het strand van het Waddeneiland Texel. RIN, Texel.
Degraer, S., Volckaert, A. & Vincx, M. (2003). Macrobenthic zonation patterns along a
morphodynamical continuüm of microtidal low tide bar/rip and ultradissipative sandy beaches.
Estuarine, Coastal and Shelf Science 56 (2003): 459-468.
De Meulenaer, B. (2006). Voedselecologie van strandvogels: Drieteenstrandloper (Calidris alba).
Licentiaatsscriptie, Universiteit Gent, Gent.
Dias, M.P., Granadeiro, J.P., Lecoq M., Santos , D.C. & Palmeirim J.M. (2006a). Distance to high-tide
roosts constrains the use of foraging areas by dunlins: Implications for the management of estuarine
wetlands. Biological conservation 131 (3): 446-452.
Dias, M.P., Granadeiro, J.P., Martins, R.C. & Palmeirim, J.M. (2006b). Estimating the use of tidal flats
by waders: inaccuracies due to the response of birds to the tidal cycle. Bird study 53: 32-38 Part 1.
Dodd, S.L. & Colwell, M.A. (1996). Seasonal variation in diurnal and nocturnal distributions of
nonbreeding shorebirds at North Humboldt Bay, California. The Condor 98: 196-207.
Dugan, P.J. (1981). The importance of nocturnal foraging in shorebirds – A consequence of increased
invertebrate prey activity. In: Feeding strategies and survival of estuarine organisms (eds. Jones, N.V.
& Wolff, W.J.), 251-260. Plenum Press, New York.
Engelmoer, M. & Roselaar, C. (1998). Geographical variation in waders. Kluwer, Dordrecht.
Engledow, H.; Spanoghe, G.; Volckaert, A., Coppejans, E.; Degraer, S; Vincx, M.; Hoffmann, M.
(2001). Onderzoek naar (1) de fysische karakterisatie en (2) de biodiversiteit van strandhoofden en
andere harde constructies langs de Belgische kust; eindrapportage. Verslag van het Instituut voor
Natuurbehoud, 2001.20. Universiteit Gent (RUG), vakgroep Biologie, Laboratorium Plantkunde: Gent.
133p.
46
Ens, B.J. & Zwarts, L. (1980). Territoriaal gedrag bij Wulpen buiten het broedgebied. Watervogels 5:
108-120.
Ens, B.J., Wintermans, G.J.M. & Smit, C.J. (1993). Verspreiding van overwinterende wadvogels in de
Nederlands Waddenzee. Limosa 66: 137-144.
Ens, B.J., Brinkman, A.G., Dijkman, E.M., Meesters, H.W.G., Kersten, M., Brenninkmeijer, A. & Twisk,
F. (2005). Modelling the distribution of waders in the Westerschelde. What is the predictive power of
abiotic variables? Alterra rapport 1193, Wageningen.
Esselink, P. (1982). De verspreiding van Wulpen (Numenius arquata) tijdens laagwater, foeragerend
op Zeeduizendpoten (Nereis diversicolor). Studentenrapport Zoölogisch Laboratorium Rijksuniversiteit
Groningen, Groningen / Rijksdienst voor de Ijselmeerpolder, Lelystad.
Esselink, P. & Zwarts, L. (1989). Seasonal trend in burrow depth and tidal variation in feeding activity
of Nereis diversicolor. Marine Ecology Progress Series 56: 243-354.
Evans, P.R. (1976). Energy balance and optimal foraging strategies in shorebirds: some implications
for their distributions and movements in the non-breeding season. Ardea 64: 117-137.
Evans, P.R., Herdson, D.M., Knights, P.J. & Pienkowski, M.W. (1979). Short-Term Effects of
Reclamation of Part of Seal Sands, Teesmouth, on wintering waders and Shelduck. I. Shorebird diets,
invertebrate densities, and impact of predation on the invertebrates. Oecologica 41: 183-206.
Evans, P.R. (1979). Adaptations shown by foraging shorebirds to cyclical variations in the activity and
availability of their intertidal invertebrate prey. In: Cyclic Phenomena in Marine Plants and Animals.
(eds. Naylor, E. & Hartnoll, R.G.), 357-366. Permagon, Oxford.
Evans, T.J. & Harris, S.W. (1994). Status and habitat use by American avocets wintering at Humboldt
Bay, California. Condor 96: 178-189.
Gerritsen, A.F.C. & Van Heezik, Y.M. (1985). Substrate preference and substrate related foraging
behaviour in three Calidris species. Netherlands Journal of Zoology 35: 671-692.
Glutz von Blotzheim, U.N., Bauer, K.M. & Bezzel, E. (1984). Handbuch der Vögel Mitteleuropas. Aula,
Wiesbaden.
Goss-Custard, J.D. (1969). The winter feeding ecology of the redshank Tringa totanus. Ibis 111: 338356.
Goss-Custard, J.D. (1970). The responses of redshank Tringa totanus to spatial variations in the
density of their prey. Journal of Animal Ecology 39: 91-113.
Goss-Custard, J.D. (1977). Predator responses and prey mortality in the redshank Tringa totanus (L.).
Journal of Animal Ecology 39: 91-113.
Goss-Custard, J.D. (1977b). Predator responses and prey mortality in redshank, Tringa totanus (L.),
and a preferred prey, Corophium volutator; Journal of Animal Ecology 46: 21-35.
Goss-Custard, J.D. (1980). Competition for food and interference among waders. Ardea 68: 31-52.
Goss-Custard, J.D. (1984). Intake rates and food supply in migrating and wintering shorebirds. In:
Behaviour of Marine Animals, Vol. 6 (eds. Burger, J. & Olla, B.L.), 233-270. Plenum Press, New York.
Goss-Custard, J.D. (1985). Foraging behaviour of wading birds and the carrying capacity of estuaries.
In: Behavioural Ecology: ecological consequences of adaptive behaviour (eds. Sibly, R.M. & Smith,
R.H.), 169-188. Blackwell Scientific Publications, Oxford.
47
Goss-Custard, J.D. (eds.) (1996). The oystercatcher. From individuals to populations. Oxford
University Press, Oxford, 442p.
Goss-Custard, J.D., Jones, R.E. & Newberry, P.E. (1977). The ecology of the Wash I. Distribution and
diet of wading birds (Charadrii). Journal of Applied Ecology 14: 681-700.
Goss-Custard, J.D. & Yates, M.G. (1992). Towards predicting the effect of salt-marsh reclamation on
feeding bird numbers on the wash.. Journal of applied Ecolgy 29: 330-340.
Goss-Custard, J.D., Stillman, R.A., West, A.D., Caldow, R.W.G., Triplet, P., Durell, S.E.A.Le V. dit &
McGrorty, S. (2004). When enough is not enough: shorebirds and shellfishing. Proceedings of the
Royal Society London B (274): 233-237.
Granadeiro, J.P., Andrade J. & Palmeirim, J.M. (2004). Modelling the distribution of shorebirds in
estuarine areas using generalised additive models. Journal of research 52 (3): 227-240.
Granadeiro, J.P., Dias, M.P., Martins, R.C. & Palmeirim, J.G. (2006). Variation in numbers and
behaviour of waders during the intertidal cycle: implications for the use of estuarine sediment flats.
Acta Oecologica 29: 293-300.
Granadeiro, J.P., Santos, C.D., Dias, M.P. & Palmeirim, J.M. (in press). Environmental factors drive
habitat partitioning in birds feeding in intertidal flats: implications for conservation.
Grant, J. (1984). Sediment microtopography and shorebird foraging. Marine Ecology - Progress Series
19: 293-296.
Graveland, J. (2005). Fysische en ecologische kennis en modellen voor de Westerschelde: wat is
beleidmatig nodig en wat is beschikbaar voor de m.e.r. Verruiming Vaargeul? Rapport RIKZ/2005.018,
Rijkswaterstaat, Rijksinstituut voor Kust en Zee, Middelburg.
Hill, D., Rushton, S.P., Clark, N. Green, P. & Prys-Jones, R. (1993). Shorebirds communities on British
estuaries: factors determining community composition. Journal of Applied Ecology 30: 220-234.
Hilton, G.M., Ruxton, D.R. & Cresswell, W. (1999). Choice of foraging area with respect to predation
risk in redshanks: the effects of weather and predator activity. Oikos 87(2): 295-302.
Höfmann, H. & Hoerschelmann, H. (1969). Nahrungsuntersuchungen bei Limikolen durch
mageninhaltsanlalysen. Corax 3: 7-22.
Hötker, H. (1999). What determines the time-activity budgets of avocets (Recurvirostra avosetta)?
Journal of Ornithology 140 (1): 57-71.
Holloway, S.J., Rehfisch, M.M., Clark, N.A., Balmer, D.E., Austin, G., Yates, M.G., Clarke, R.T.,
Swetnam, R.D., Eastwood, J.A., Durell, S.E.A. le V. dit, Goss-Custard, J.D. & West, J.R. (1996).
Estuary, Sediments and Shorebirds II. Shorebird Usage of Intertidal Areas. BTO Research Report
(ETSU Project T/04/00206/REP). ETSU, Harwell.
Hulscher, J.B. (1976). Localisation of cockles Cardium edule L. by the oystercatcher Haematopus
ostralegus in darkness and daylight. Ardea 64: 292-310.
Hulscher, J.B. (1996). Food and feeding behaviour. In: The oystercatcher. From individuals to
populations (eds. Goss-Custard, J.D.), 8-29. Oxford University Press, Oxford.
Kalejta, B. (1992). Time budgets and predatory impacts of waders at the Berg River Estuary, South
Africa. Ardea 80: 327-342.
Kalejta, B. & Hockey, P.A.R. (1991). Distribution, abundance and productivity of benthic invertebrates
at the Berg River Estuary, South Africa. Estuarine Coastal Shelf Science 33: 175-191.
48
Kalejta, B. & Hockey, P.A.R. (1993). Distribution of shorebirds at the Berg River Estuary, South Africa,
in relation to foraging mode, food supply and environmental features. Ibis 136: 233-239.
Kater, B.J. (2005). Ontwikkelingen in de kennis van de morfodynamica en ecologie van de
Westerschelde. Rapport RIKZ/2005.034. Rijkswaterstaat Rijksinstituut voor Kust en Zee, Middelburg.
Kelsey, M.G. & Hassall, M. (1989). Patch selection by dunlin on a heterogeneous mudflat. Ornis
Scandinavica 20 (4): 250-254.
Lange, G. (1968). Uber Nahrung, Nahringsaufnahme und Verdauungstrakt mitteleuropaischer
Limikole. Beitr. Vogelkunde 13: 225-334.
Leopold, L.B., Collins, J.N. & Collins, L.M. (1993). Hydrology of some tidal channels in estuarine
marshland near San Fransisco. Catena 20: 469-493.
Leopold, M.F., Smit, C.J., Goedhart, P.W., van Roomen, M., van Winden, A.J. & van Turnhout, C.
(2004). Langjarige trends in aantallen wadvogels, in relatie tot de kokkelvisserij en het gevoerde beleid
in deze. Eindverslag EVA II (Evaluatie schelpdiervisserij tweede fase). Deelproject C2. Alterra-rapport
954; SOVON-onderzoeksrapport 2004/07. Alterra, Wageningen.
Leyrer, J., Spaans, B., Camara, M. & Piersma, T. (2006). Small home ranges and high site fidelity in
red knots (Calidris c. canutus) wintering on the banc d' Arguin, Mauritania. Journal of Ornithology 147:
376-384.
Lourenço, P.M., Granadeiro, J.P & Palmeirim, J.M. (2005). Importance of drainage channels for wader
foraging on tidal flats: relevance for the management of estuarine wetlands. Journal of Applied
Ecology 42: 477-486.
Madon, P. (1935). Contribution à l’étude de régime des oiseaux aquatiques. I Charadriiformes. Alauda
7: 60-84
McCulloch, & Clark, N.A. (1992). Habitat Utilisation by dunlin on British Estuaries. BTO Research
report 86.
Meire, P. (1993). Wader populations and macrozoobenthos in a changing estuary: the Oosterschelde
(the Netherlands). PhD Thesis, University of Ghent, Ghent / Institute of Nature conservation, Hasselt.
Report nr. 93.05, 311p.
Minton, C.D.T. (1975). The waders of the Wash – ringing and biometric studies. Report of the scientific
study, Wash Water storage scheme feasibility study to the natural environment Research Council.
Moreira, F. (1993). Macrohabitat selection by waders in the Tagus estuary (Portugal). Portugaliae
Zoologica 2: 1-15.
Moreira, F. (1995). The winter feeding ecology of avocets Recurvirostra avosetta on intertidal areas. I.
Feeding strategies. Ibis 137: 92-98.
Moreira, F. (1999). On the use by birds of intertidal areas of the Tagus estuary: implications for
management. Aquatic ecology 33: 301-309.
Mouritsen, K.N. & Jensen, K.T. (1992). Choice of microhabitat in tactile foraging dunlins Calidris alpina
the importance of sediment penetrability Marine Ecology - Progress Series 85 (1-2): 1-8.
Mouritsen, K.N. (1994). Day and Night feeding in dunlins Calidris alpina: choice of habitat foraging
technique and prey. Journal of Avian biology 25: 55-62.
Myers, J.P., Williams, S.L. & Pitelka, F.A. (1980). An experimental analysis of prey availability for
sanderlings (Aves:Scolopacidae) feeding on sandy beach crustaceans. Canadian Journal of Zoology
58: 1564-1574.
49
Nehls, G. & Tiedemann, R. (1993). What determines the densities of feeding birds on tidal flats-a case
study on dunlin Calidris alpina in the Wadden sea. Netherlands journal of sea research 31 (4): 375384.
Ntiamoa-Baidu, Y., Piersma, T., Wiersma, P., Poot, M., Battley, P. & Gordon, C. (1998). Water depth
selection, daily feeding routines and diets of waterbirds in coastal lagoons in Ghana. Ibis 140: 89-103.
Perez-Hurtado, A., Goss-Custard, J.D. & Garcia, F. (1997). The diet of wintering waders in Cadiz Bay,
southwest Spain. Bird Study 44: 45-52.
Perkins, E.J. (1958). The hardness of the shore at Whitstable, Kent. Journal of Ecology 46: 71-81.
Pienkowski, M.W. (1980). Aspects of the ecology and behaviour of ringed and grey plovers,
Charadrius hiaticula and Pluvialis squatarola. Unpublished PhD. Thesis, University of Durham.
Pienkwoski, M.W. (1981). How foraging plovers cope with environmental effects on invertebrate
behaviour and availability. In: Feeding strategies and survival of estuarine organisms (eds. Jones,
N.V. & Wolff, W.J.), 179-192. Plenum Press, New York.
Pienkowksi, M.W. (1982). Diet and energy intake of grey and ringed plovers, Charadrius hiaticula and
Pluvialis squatarola, in the non-breeding season. Journal of Zoology 197: 511-549.
Pienkowski, M.W. (1983). The effects of environmental conditions on feeding rates and prey-selection
of shore plovers. Ornis Scandinavica 14: 227-238.
Piersma, T., Hoekstra, R., Dekinga, A., Koolhaas, A., Wolf, P., Battley, P. & Wiersma, P. (1993). Scale
and intensity of intertidal habitat use by knots Calidris canutus in the western Wadden Sea in relation
to food, friends and foes. Netherlands Journal of Sea Research 31: 331-357.
Piersma, T., Koolhaas, A. & Dekinga A. (1993b). Interactions between stomach strucutre and diet
choice in shorebirds. Auk 110: 552-564.
Piersma, T., van Aelst, R., Kurk, K., Berkhoudt, H. & Maas, L.R. (1998). A new pressure sensory
mechanism for prey detection in birds: the use of principles of seabed dynamics. Proceeding of the
Royal Society of London B 265: 1377-1383.
Pieters, T., Storm, C. & Walhout, T. (1991). Het schelde-estuarium, meer dan een vaarweg:
rapportage pilootstudie ontwikkeling van fysische structuur van schelde-estuarium, uitgevoerd door
projectgroep oostwest. Ministerie van Verkeer en Waterstaat, notanummer, 91.081. Ministerie van
Verkeer en Waterstaat, Directoraat-Generaal Rijkswaterstaat (RWS), Dienst Getijdewateren (DGW).
Middelburg. 135p.
Prater, A.J. (1972). The ecology of Morecambe Bay. The food and feeding habits of the knot (Calidris
canutus L.) in Morecambe Bay. Journal of Applied Ecology 9: 179-194.
Puttick, G.M. (1979). Foraging behaviour and activity budgets of curlew sandpipers. Ardea 67: 111122.
Puttick, G.M. (1984). Foraging and activity patterns in wintering shorebirds. In: Behaviour of Marine
Animals, Vol. 6 (eds. Burger, J. & Olla, B.L.), 203-231. Plenum Press, New York.
Pye, K. (1992). Saltmarshes on the barrier coastline of North Norfolk, eastern England. In:
Saltmarshes: morphodynamics, conservation and engineering significance (eds. Allen, J.R.L. & Pye,
K.), 148-178. Cambridge University Press, Cambridge.
Quammen, M.L. (1982). Influence of Subtle Substrate Differences on feeding by shorebirds on
intertidal mudflats. Marine Biology 71: 339-343.
Quammen, M.L. (1984). Predation by shorebirds, fish, and crabs on invertebrates in intertidal
mudflats- an experimental test. Ecology 65: 529-537.
50
Ravenscroft, N.O.M. & Beardall, C.H. (2003). The importance of freshwater flows over estuarine
mudflats for wintering waders and wildfowl. Biological Conservation 113: 89-97.
Recher, H.F. (1966). Some aspects of the ecology of migrant shorebirds. Ecology 22: 157-174.
Rehfisch, M.M., Clark, N.A., Langston, R.H.W. & Greenwood, J.J.D.G. (1996). A guide to the provision
of refuges for waders: an analysis of 30 years of ringing data from the Wash, England. Journal for
Applied Ecology 31: 383-401.
Rehfisch, M.M., Insley, H. & Swann, B. (2003). Fidelity of overwintering shorebirds to roosts on the
moray basin, Scotland: implications for predicting impact of habitat loss. Ardea 91(1): 53-70.
Ribeiro, P.D., Iribarne, O.O., Navarro, D. & Jaureguy, L. (2004). Environmental heterogeneity, spatial
segregation of prey, and the utilization of southwest Atlantic mudflats by migratory shorebirds. Ibis
146: 672-682.
Rogers, D.I., Battley, P.F., Piersma, T., van Gils, J. & Rogers, K.G. (2006). High tide habitat choice:
insights from modelling roost selection by shorebirds around a tropical bay. Animal Behaviour, in
press.
Rosa, S., Palmeirim, J.M. & Moreira, F.(2002). Factors influencing waterbird abundance and Species
richness in an increasingly urbanised area of the Tagus Esuary in Portugal. Waterbirds 26(2): 226232.
Roukema, B. (1984). Exploitatie van Arenicola door de Wulp: het problem van prooibeschikbaarheid.
Studentenrapport Zoölogisch Laboratorium Rijksuniversiteit Groningen / Rijksdienst voor de
IJsselmeerpolder, Lelystad.
Ruiters, P.S. (1992). Relaties tussen verspreiding en dieetkeuzes van steltlopers en het voorkomen
van macrozoobenthos in de Westerschelde. Rapporten en verslagen NIOO 1992-04, Yerseke, 49p.
Scheiffarth, G. (2001). The diet of bar-tailed godwits Limosa lapponica in the Wadden Sea: combining
visual observations and faeces analyses. Ardea 89(3): 481-494.
Sitters H.P., González P.M., Piersma, T., Baker, A.J. & Price, D.J. (2000). Day and night feeding
habitat of red knots in Patagonia: profitability versus safety. Journal of Field Ornithology 72(1): 86-95.
Smit, C.J. & Wolff, W.J. (1981). Birds of the wadden sea: final report of the section “birds” of the
wadden sea working group. A.A. Balkema, Rotterdam. 308p.
Smith, P.C. & Evans, P.R. (1973). Studies of shorebirds at Lindisfarme, Northumberland. I. Feeding
ecology and behaviour of the bar-tailed godwit. Wildfowl 124: 135-139.
Smith, P.C. (1975). A study of the winter feeding ecology and behaviour of the bar-tailed godwit
(Limosa lapponica). Unpublished PhD. Thesis, University of Durham, UK.
Speybroeck, J., Bonte, D., Grootaert, P., Maelfait, J.P., Stienen, E.W.M., Vandomme, V., Vanermen,
N., Vincx, M. & Degraer, S. (2006). Studie over de impact van zandsuppleties op het ecosysteem Fase 2. Universiteit Gent, dossiernr. 204.295.
Stillman, R.A., West, A.D., Goss-Custard, J.D., Caldow, R.W.G., McGrorty, S., Durell, S.E.A.Le V.Dit.,
Yates, M.G., Watkinson, P.W., Clark, N.A., Bell, M.C.., Dare, P.J. & Mander, M. (2003). An individual
behaviour-based model can predict shorebird mortality using routinely collected shellfishery data.
Journal of Applied Ecology 40: 1090-1101.
Stillman, R.A., West, A.D., Goss-Custard, J.D., McGrorty, S., Frost, N.J., Morrisey, D.J., Kenny, A.J. &
Drewitt, A.L. (2005). Predicting site quality for shorebird communities: a case study on the Humber
estuary. Marine Ecology Progress Series 305: 203-217.
51
Stillman, R.A. & Goss-Custard, J.D. (2006). Using behavior to predict the effects of environmental
change on shorebirds during the non-breeding season. Acta Zoologica 52: 536-540.
Summers, R.W., Underhill, L.G. & Simpson, A. (2002). Habitat preferences of waders (Charadrii) on
the coast of the Orkney islands. Bird Study 49: 60-66.
Sutherland, W.J. (1982). Do oystercatchers select the most profitable cockles? Animal Behaviour 30:
857-861.
Symonds, F.L., Langslow, D.R. & Pienkowski, M.W. (1984). Movements of wintering shorebirds within
the firth of forth-species-differences in usage of an intertidal complex Biological conservation 28 (3):
187-215.
Tjallingii, S.J. (1972). Habitat selection of the Avocet (Recurvirostra avocetta) in relation to feeding. In:
Voous, K.H. (ed.) Proc. XVth International Congres E.J.Brill, London, 696-697.
Thompson, D.B.A., Curtis, D.J. & Smyth, J.C. (1986). Patterns of association between birds and
invertebrates in the Clyde estuary. Proceedings of the Royal Society of Edinburgh 90B: 185-201.
Thrush, S.F. (1991). Spatial patterns in Soft-bottom communities. Tree 6(3): 75-78.
Townshend, D.J. (1981). The importance of field feeding to the survival of wintering male and female
curlews Numenius arquata on the Tees estuary. In: Feeding and survival strategies of Estuarine
organisms (eds. Jones, N.V. & Wolff, W.J.), 261-273. Plenum Press, New York.
Townshend, D.J., Dugan, P.J. & Pienkowski, M.W. (1984). The unsociable plover – use of intertidal
areas by grey plovers. In: Coastal Waders and wildfowl in winter (eds. Evans, P.R., Goss-Custard,
J.D. & Hale, W.G.), 140-159. Cambridge University Press, Cambridge.
Tulp, I. & de Goeij, P. (1994). Evaluating wader habitats in Roebruck Bay (North-western Australia) as
a springboard for nothbound migration in waders, with a focus on great knots. EMU 94: 78-95.
van de Kam, J., Ens, B., Piersma, T., Zwarts, L. (1999). Ecologische atlas van de Nederlandse
Wadvogels. Schuyt en co., Haarlem, 368p.
Van Eck, B. (2006). Monitoring VErruiming WEsterschelde, MOVE Eindrapportage, Eindconcept
augustus 2006. Rijkswaterstaat Rijkinstituut voor Kust en Zee, Middelburg.
van Gils, J.A., Piersma, T., Dekinga, A. & Dietz, M.W. (2003). Cost-benefit analysis of mollusc-eating
in a shorebird. II. Optimising gizzard size in the face of seasonal demands. Journal of experimental
Biology 206: 3369-3380.
van Gils, J.A., Edelaar, P., Escudero, G. & Piersma, T. (2004). Carrying capacity models should not
use fixed prey density thresholds: a plea for using tools of behavioural ecology. Oikos 104(1): 197204.
Van Gils, J.A., De Rooij, S.R., Van Belle, J., Van der Meer, J., Dekinga, A., Piersma, T. & Drent, R.
(2005a). Digestive bottlenecks affects foraging decisions in red knots Calidris canutus. I. Prey choice.
Journal of Animal Ecology 74: 105-119.
van Gils, J.A., Dekinga, A., Spaans, B., Vahl, W.K. & Piersma, T. (2005b). Digestive bottlenecks
affects foraging decisions in red knots Calidris canutus. II. Patch choice and length of working day.
Journal of Animal Ecology 74: 120-130.
van Gils, J.A., Spaans, B., Dekinga, A. & Piersma, T. (2006). Foraging in a tidally structures
environment by red knots (Calidris canutus): ideal, but not free. Ecology: 87(5): 1189-1202.
van Kleunen, A. (1999). Verspreiding en habitatvoorkeur van eenden en steltlopers in de Ooster- en
Westerschelde op basis van laagwater vogelkartering in januari en februari 1990. Werkdocument
RIKZ/OS/2000.806X.
52
van Turnhout, C. & van Roomen, M. (2005). Effecten van strandsuppleties langs de Nederlandse kust
op Drieteenstrandloper en kustbroedvogels SOVON-onderzoeksrapport 2005/5 SOVON
vogelonderzoek Nederland, Beek-Ubbergen
Velásquez, C.R. & Navarro, R.A. (1993). The influence of water depth and sediment type on the
foraging behaviour of Whimbrels. Journal of Field Ornithology 64(2): 149-157.
Vroon, J., Storm, C. & Coosen, J. (1997). Westerschelde, stram of struis? Eindrapport van het Project
Oostwest, een studie naar de beïnvloeding van fysische en verwante biologische patronen in een
estuarium. Rapport RIKZ-97.023.
Warwick, R.M., Goss-custard, J.D., Kirby, R., George, C.L., Pope, N.D. & Rowden, A.A. (1991). Static
and dynamic environmental factors determining the community structure of estuarine macrobenthos in
SW Britain: why is the Severn estuary different? Journal of Applied Ecology 28: 329-345.
Weber, L.M. & Haig, S.M. (1996). Shorebird use of South Carolina managed and natural coastal
wetlands. Journal of wildlife management 60 (1): 73-82.
Whitfield, D.P. (2003). Redshank Tringa totanus flocking behaviour, distance from cover and
vulnerability to sparrowhawk Accipter nisus predation. Journal of avian biology 34:163-169.
Wolff, W.J. (1969). Distribution of non-breeding waders in an estuarine area in relation to the
distribution of their food organisms. Ardea 57: 1-28.
Yates, M.G., Goss-Custard, J.D., McGrorty, S., Lakhani, K.H., Durell, S.E.A.LeV.Dit., Clarke, R.T.,
Rispin, W.E., Moy, I., Yates, T., Plant, R.A. & Frost, A.J. (1993). Sediment characteristics, invertebrate
densities and shorebird densities on the inner banks of the Wash. Journal of Applied Ecology 30: 599614.
Yates, M.G., Clarke, R.T., Swetman, R.D., Eastwood, J.A., Durell, D.E.A.le V.dit., West, J.R., Gosscustard, J.D., Clark, N.A., Holloway, S.J. & Rehfisch, M.M. (1996). Estuary Sediments and Shorebirds
I. Determinants of the Interidal sediments of Estuaries. BTO- research-Report (ETSU
T/04/00205/REP) ETSU, Harwell.
Ysebaert, T., Meininger, P.L., Meire, P., de Vos, K., Berrevoets, C.M. Strucker, R.C.W. & Kuijken, E.
(2000). Waterbird communities along the estuarine salinity gradient of the Schelde estuary, NWEurope. Biodiversity and conservation 9: 1275-1296.
Zwarts, L. (1974). Voedselopname en foerageergedrag van Tureluurs op het wad onder
Schiermonnikoog. Schierboek 5: 183-227.
Zwarts, L. (1981). Habitat selection and competition in wading birds. In: Birds of the Wadden Sea
(eds. C.J. Smit & W.J. Wolff), 271-279. A.A. Balkema, Rotterdam.
Zwarts, L. (1988a). Numbers and distribution of coastal waders in Guinee-Bissau. Ardea 76: 42-55.
Zwarts, L. (1988b). De bodemfauna van de Fries-Groningse waddenkust. Flevobericht 294.
Rijksdienst voor de Ijselmeerpolders, Lelystad.
Zwarts, L. (1996a). Met hoogwatertellen alleen kom je er niet. Limosa 69: 142-145.
Zwarts, L. (1996b). Waders and their estuarine food supplies. Proefschrift Rijksuniversiteit Groningen,
Groningen, 386p.
Zwarts, L. & Wanink, J. (1984). How oystercatchers and curlews successively deplete clams. In:
Coastal waders and wildfowl in winter (eds. Evans, P.R., Goss-Custard, J.D. & Hale, W.G.), 69-83.
Cambridge University Press, Cambridge.
53
Zwarts, L. & Esselink, P. (1989). Versatility of male curlews Numenius arquata preying upon Nereis
diversicolor: deploying contrasting capture modes dependent on prey availability. Marine Ecological
progress Series 56: 255-269.
Zwarts, L. & Blomert, A.M. (1992). Why knot Calidris canutus take medium-sized Macoma Balthica
when six prey species are available. Marine Ecology Progress Series 83: 113-128.
Zwarts, L. & Wanink, J.H. (1993). How the food supply harvestable by waders in the Wadden Sea
depends on the variation in energy density, body weight, biomass, burying depth and behaviour of
tidal-flat invertebrates. Netherlands Journal of Sea Research 31(4): 441-476.
Zwarts, L., Blomert, A. & Hupkes, R. (1990). Increase of feeding time in waders preparing for spring
migration from the Banc d’ Arguin, Mauritania. Ardea 78: 237-256.
Zwarts, L., Blomert, A.M. & Wanink, J.H. (1992). Annual and seasonal variation in the food supply
harvestable by knot Calidris canutus staging in the Wadden Sea in late summer. Marine Ecology
Progress Series 83: 129-139.
Zwarts, L., Wanink, J.H. & Ens, B.J. (1996). Predicting seasonal and annual fluctuations in the local
exploitation of different prey by oystercatchers Haematopus ostralegus: a ten year study in the
Wadden Sea. Ardea 84A: 401-440.
54
APPENDIX I
Following graphs summarise the data obtained by van Kleunen (1999) in the Westerschelde. The left
graphs show the relation between bird densities (number/ha) and the silt content (particles <64µm) of
the soil (%). The graphs on the right present the relation between bird densities and the time the area
is exposed (as a percentage of the 12,5 hour tidal cycle). One of the disadvantages of the dataset
obtained by van Kleunen (1999) is that the study areas used were not homogenous in terms of
sediment characteristics.
Oystercatcher:
Avocet:
Grey plover:
55
Knot:
Sanderling:
Dunlin:
56
Bar-tailed godwit:
Curlew:
Redshank:
57
Turnstone:
58
APPENDIX II: Shorebird rankings according habitat preferences
Table 6. Bird species ranked according to their preference from sandy to muddy substrates in four different
estuaries.
Waddenzee
Guinea-Bissua
Tagus estuary
Westerschelde
Moreira (1999)
(Van Kleunen, 1999, (Zwarts, unpublished (Zwarts et al., 1988a)
data, in: Blomert,
in: Blomert, 2002)
2002)
oystercatcher
3
3
2
avocet
9
11
10
ringed plover
4
10
2
Kentish plover
7
4
grey plover
5
8
8
8
knot
2
7
4
7
sanderling
1
1
1
dunlin
7
6
5
bar-tailed godwit
6
2
3
6
curlew
4
5
6
3
spotted redshank
10
redshank
8
9
5
9
turnstone
10
1
9
Table 7. Bird species ranked according to their preference from low to high intertidal areas in two different
estuaries.
Westerschelde
Waddenzee
(Van Kleunen, 1999,
(Zwarts, unpublished
in: Blomert, 2002)
data, in: Blomert,
2002)
oystercatcher
avocet
ringed plover
Kentish plover
grey plover
knot
sanderling
dunlin
bar-tailed godwit
curlew
spotted redshank
redshank
turnstone
5
9
3
6
11
6
8
7
10
4
3
9
8
1
2
7
2
4
10
5
1
59
60
APPENDIX III: Question Form
When answering this survey, please keep in mind that only intertidal flats are dealt with. Please
answer the questions according to your own experience and to the situation in your own study area,
irrespective of the specific (and possibly different) situation in the Westerschelde. However, even if
you are not familiar with some of the mentioned shorebird species, please do include them in the
rankings as this is important for further analysis.
1) Sediment
Sediment influences shorebird distribution in several manners. Most importantly, sediment type has a
direct impact on the macrobenthos community, both on diversity and densities of benthos, as on the
availability of this food source for shorebirds.
•
•
•
Classify the birds according to their sediment preference: do this by assigning number 1 to the
species with the strongest preference for sandy sediments, and number 13 to the species with
the strongest preference for muddy sediments.
Describe the preferred sediment for each species, using only the following three categories:
sandy, intermediate, muddy.
Range: this column is added to get an idea of the dependency of the shorebirds on the preferred
substrate:
1 = the birds forage nearly exclusively on their favoured sediment type
2 = the birds forage mostly on their favoured sediment type
3 = the birds forage on a broad range of sediment types, with a slight preference for the
favoured sediment type
Table 1. Sediment preference of 13 species of waders .
Sort by sediment
Describe sediment
preference
type
oystercatcher
avocet
ringed plover
Kentish plover
grey plover
knot
sanderling
dunlin
bar-tailed godwit
curlew
spotted redshank
redshank
turnstone
Range
61
2) Emersion time
Emersion time has an important influence on the distribution of birds on mudflats. First of all, the
emersion time stipulates the availability of the flat to waders and consequently, determines the total
carrying capacity of a certain area. Secondly, emersion time has an influence on the prey density as
well as on the availability of this prey (Yates et al., 1993; Blomert, 2002; Granadeiro et al., 2003;
Graveland, 2005).
•
•
Please sort the following species according to their preferred part of the intertidal. The number 1
is given to the species that favours most the lowest part (short emersion time), and number 13 is
given to the species that favours most the highest part of the intertidal (long emersion time).
Counts performed during low tide underestimate the use of the high-tidal areas. This is because
some species are strongly associated with the waterline so it seems that during low tide counts
they prefer the low intertidal zone while in fact they use the whole intertidal equally. Thompson et
al., (1986); Nehls & Tiedemann, (1993); van de Kam et al., (1999); Danufsky & Colwell, (2003)
and Granadeiro et al. (2006) separate shorebirds in so-called “followers” and “non-followers” to
distinguish between waders that follow the tide line and those that do not. Can you tell us,
according to your experience, if these species are:
FO =
NF =
?=
Followers
Non-followers
No idea
Table 2. Emersion time preference of 13 species of wader.
Sort according to
Follower /
exposure time
Non-follower
oystercatcher
avocet
ringed plover
Kentish plover
grey plover
knot
sanderling
dunlin
bar-tailed godwit
curlew
spotted redshank
redshank
turnstone
62
3) Prey-choice and specificity
Highly specialised species are likely to be less flexible in their foraging behaviour.
•
•
•
We first would like you to assign a code indicating the flexibility in prey choice:
0 = great flexibility, can easily switch to other food sources,
1 = quite flexible, preys on a rather broad range of prey,
2 = very strong preference for certain prey; (almost) no alternative prey.
In the second column please enter the most targeted prey (species or higher taxon) for each bird
species.
In the third column you may indicate how abiotic factors determine the presence of their favoured
prey: sediment preference (sandy, intermediate, muddy), tidal zone preference (high, mid, low
tidal)
Tabel 3. Prey specifity and prey choice of 13 species of wader.
Prey specifity
Favoured prey
Habitat preference of
favoured prey
oystercatcher
avocet
ringed plover
Kentish plover
grey plover
knot
sanderling
dunlin
bar-tailed godwit
curlew
spotted redshank
redshank
turnstone
4) Other abiotic factors
Do you believe there are other important (abiotic) factors (apart from salinity, emersion time and
sediment) affecting shorebird distribution in estuaries?
5) Remarks and recommendations
Do you have any remarks or recommendations that could be important for the continuation of this
survey?
63