Ocean & Coastal Management 68 (2012) 79e88

Contents lists available at SciVerse ScienceDirect

Ocean & Coastal Management

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

Signals from the Wadden sea: Population declines dominate among waterbirds depending on intertidal mudflats

Marc van Roomen a,*, Karsten Laursen b, Chris van Turnhout a, Erik van Winden a, Jan Blew c, Kai Eskildsen d, Klaus Günther e, Bernd Hälterlein d, Romke Kleefstra a, Petra Potel f, Stefan Schrader g, Gerold Luerssen h, Bruno J. Ens a a SOVON Dutch Centre For Field Ornithology, P.O. Box 6521, 6503 GA Nijmegen, The Netherlands b Department of Bioscience, Aarhus University, Grenaavej 12, DK-8410 Roende, Denmark c BioConsult SH, Brinckmannstr. 31, 25813 Husum, Germany d Nationalparkverwaltung Schleswig-Holsteinisches Wattenmeer, Schlossgarten 1, D-25832 Tönning, Germany e Schutzstation Wattenmeer, Nationalpark-Haus, Hafenstrasse 3, D-25813 Husum, Germany f Nationalparkverwaltung Niedersächsisches Wattenmeer, Virchowstrasse 1, D-26382 Wilhelmshaven, Germany g Landesbetrieb für Küstenschutz, Nationalpark und Meeresschutz Schleswig-Holstein, Herzog-Adolf Strasse 1, D-25813 Husum, Germany h Common Wadden Sea Secretariat, Virchowstrasse 1, D-26382 Wilhemshaven, Germany article info abstract

Article history: The Wadden Sea, shared by Denmark, Germany and the Netherlands, is one of the world’s largest Available online 12 April 2012 intertidal wetlands. Waterbirds are an important element of the Wadden Sea ecosystem. By their migratory behaviour they connect the Wadden Sea with other sites, ranging from the arctic to the western seaboards of Europe and Africa, forming the East-Atlantic Flyway. The Joint Monitoring of Migratory Birds (JMMB) project of the Trilateral Monitoring and Assessment Program (TMAP) follows the changes in population size within the Wadden Sea. In this paper we describe and analyse population trends over the years 1991e2009 for 22 waterbird species using the Wadden Sea in internationally important numbers and depending on intertidal mudflats. Population declines predominated in this 18- year period. More populations decreased in Schleswig-Holstein and Niedersachsen than in The Netherlands and Denmark. This is the case particularly for species feeding on polychaetes. In contrast, waterbirds feeding on bivalves are in decline in all regions except Denmark. On the finer spatial scale of tidal basins, these patterns in trends are still apparent, although much variation in trend directions exists within the Dutch Wadden Sea, especially in bivalve specialists. For those species for which we could compare the trend in the Wadden Sea with the trend of their entire flyway population, we found that the former were more negative. This finding and the contrasting trends between regions and tidal basins within the Wadden Sea suggest that causes of the population changes are to be sought within the Wadden Sea itself. These causes, which may act in combination, could be related to factors operating within the Wadden Sea only or with factors operating on a larger scale but having an intensified or differentiated effect within the Wadden Sea. Interestingly, the Wadden Sea regions where negative trends of benthivorous waterbirds predominate are characterized by a large tidal amplitude, whereas areas where bird numbers have generally increased are characterized by a small tidal amplitude. An inventory of possible causes indicated climate change, eutrophication, shellfish fisheries, invasive species and increasing numbers of avian predators as the most important candidates to be investigated further to explain the observed trends. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction

The Wadden Sea, shared by Denmark, Germany and the Netherlands, constitutes one of the world’s largest intertidal wetlands, providing a wide range of ecosystem services and sup- * Corresponding author. porting many conservation interests (Marencic and De Vlas, 2009). E-mail address: [email protected] (M. van Roomen). It is designated as a UNESCO World Heritage site (for the

0964-5691/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ocecoaman.2012.04.004 80 M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88

Netherlands and Germany), Natura 2000 site and a site of inter- 2. Material and methods national importance under the Ramsar convention. It is managed according to the trilateral Wadden Sea Plan (WSP), which provides 2.1. Study site and species selection a coordinated framework for the management principles and the implementation of national and international legislation. Biolog- The Wadden Sea is a large (14,700 km2) shallow tidal wetland, ical, environmental and socio-economic parameters are monitored containing more than 4500 km2 of soft-sediment flats that emerge within the Trilateral Monitoring and Assessment Program (TMAP) twice a day during low tide (Laursen et al., 2010). Large numbers of to provide baseline information for policy and management. waterbirds use these tidal flats for foraging and roost on nearby salt- Despite strong legal protection and many management measures marshes, polders and islands during high-tide. In this paper we being in place, conflicts between human use and conservation distinguish four regions within the Wadden Sea: Denmark, Schleswig- interests occur on a regular basis. At the same time, scientists Holstein and Niedersachsen/Hamburg (both being part of Germany) disagree on the main drivers affecting this ecosystem (Philippart and The Netherlands (Fig.1). Secondly, tidal basins are distinguished to et al., 2007; Eriksson et al., 2010). calculate trends at smaller spatial scales (based on Kraft et al., 2011;see Waterbirds constitute a visible and important element of the Fig. 1). A tidal basin comprises those areas that are influenced by the Wadden Sea ecosystem (Meltofte et al., 1994; Van de Kam et al., tide from one specific tidal inlet, so form a geographical unit influ- 2004). The international designations of the Wadden Sea are enced by the same hydrodynamic and geomorphological factors. largely based on its significance for migratory waterbirds. At least The analyses in this paper focus on 22 waterbird species 52 populations of 41 species, breeding from Canada in the west to occurring in internationally important numbers in the Wadden Sea Siberia in the east and wintering along the western coasts of Europe and largely depending on the macrobenthos of intertidal flats and Africa, use the Wadden Sea in internationally important (Table 1). The Common Eider is included in this selection as well, as numbers (defined as the regular occurrence of 1% or more of their it depends on the same macrofauna although largely from the flyway or biogeographical population; Wetlands International, sublitoral. Calculations of maximum numbers in the Wadden Sea 2006) during longer or shorter parts of their annual cycle and their international importance are based on Laursen et al. (Meltofte et al., 1994). Systematic counts of waterbirds have been (2010). For species with more than one flyway population using conducted since the 1960s in the various Wadden Sea countries the Wadden Sea, numbers for the population for which the Wadden (Smit and Wolff, 1981). Since the beginning of the 1990’s these Sea has the highest international importance was used. counts are coordinated within the Joint Monitoring of Migratory Birds (JMMB) project within TMAP (Rösner, 1993). Since its incep- 2.2. Waterbird counts and trend analyses tion, the JMMB has made much progress, allowing meaningful analyses and comparisons of trends (Blew et al., 2007; Laursen Counts of numbers of waterbirds on high-tide roosts are used to et al., 2010). Nowadays, trends for 34 waterbird species are upda- calculate population trends as collected with the JMMB project (see ted annually (JMMB, 2010). The monitoring project has mainly Rösner, 1993; Blew et al., 2007 and Laursen et al., 2010 for details). a signalling function, needed for the assessment of the conservation Three types of counts are used in the present analyses: 1) simul- status of the species of interest. Secondly, waterbirds are also taneous total counts covering all high-tide roosts of all waterbird excellent indicators of changes in the habitats they frequent, species (two counts a year are organised on the trilateral level, because of their high position in the food chain (Furness and involving 688 counting units, and up to three additional counts on Greenwood, 1993). regional level), 2) frequent counts (at least once a month) of all In this paper we present and analyse population trends since waterbird species in a selection of 163 counting units, 3) dedicated 1991 of those waterbird species that depend on intertidal mudflats aerial counts of Common Eiders in the total Wadden Sea in January for their feeding. Intertidal mudflats are the main feeding habitat (Laursen et al., 2010). for a large proportion of the waterbird species in the Wadden Sea. Trend analyses are performed on yearly indices for the total The year 1991 is taken as the starting year because this season Wadden Sea, separate regions or tidal basins. Yearly indices are marks an all-time low in the abundance of bivalves, particularly based on monthly averages, being the sum of numbers counted Mussels Mytilus edulis, in the Wadden Sea (Ens, 2006; Kristensen plus numbers estimated for units with missing counts in JulyeJune and Borgstrøm, 2006; Nehls et al., 2009a). Mussels and the beds divided by 12. The use of 12 months in these yearly indices adds they form are an important feature of mudflats providing food for robustness to the index and combines several functional periods several species and creating a suitable habitat for others, both on (migration, wintering, moult) for the same species. Accounting for the beds themselves and in the immediate surrounding (Ens et al., missing counts is done with UINDEX (Bell, 1995), on the basis of 2004; Piersma and Koolhaas, 1997). After 1991, new management site, month and year factors estimated from the non-missing measures were introduced to protect stocks of mussels and other counts (Underhill and Prys-Jones, 1994). For this, counting units bivalves against overexploitation (Ens et al., 2004; Nehls et al., are grouped in regional strata. For Common Eider only, January 2009b). It is of interest to see how waterbirds depending on counts constitute the yearly indices. The yearly indices are analysed these bivalves and/or associated habitats developed since then. We for linear trends using log-linear Poisson regression, as imple- start with analysing the number of mudflat-dependent bird species mented in the TRIM software (Pannekoek & van Strien, 2001). in the Wadden Sea as a whole, providing insight in the conservation Significance of linear trends is tested with Wald-tests. Linear trends status of these species since 1991. These trends will be compared are expressed as a single estimate (with standard error) repre- with population trends in the entire flyway of the species, to senting the average annual proportional increase or decrease in explore whether trends are specific to the Wadden Sea or part of numbers over the entire period. a broader development. Secondly, we will investigate these trends in more detail, both by looking at different spatial scales (countries/ 2.3. Comparative analysis between species and spatial scales regions and tidal basins within the Wadden Sea, Fig. 1) and at species groups with different diets (i.e. polychaetes or bivalves). In Trends in the Wadden Sea are compared with trends at the the discussion, we review possible environmental drivers affecting flyway level for 11 populations (Nagy et al., 2012). To compare the these population trends and assess their role in explaining the trend of the flyway population with that for the same population in observed patterns. the Wadden Sea, subspecies-specifi c Wadden Sea trends were M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88 81

Fig. 1. The Wadden sea, with the regions and tidal basins as used in current analyses (from Kraft et al., 2011). The extent of littoral mudflats is also indicated.

Table 1 Species analysed in this paper. Given are the average peak numbers in the Wadden sea in the period 1999/00e2006/07 (based on Laursen et al., 2010), the percentage of the total flyway population occurring in the Wadden sea at that peak moment (flyway population size based on Wetlands International, 2006) and the feeding guilds the species belong to (based on Leopold et al., 2004). For wader species with more than one flyway population occurring in the Wadden sea, numbers are given for the population with the largest international significance.

Common names Scientific names Average piek nr. in Wadden sea Percentage of flyway Food choice population in Wadden sea Common Shelduck Tadorna tadorna 246,000 82 Mixed benthos Common Eider Somateria mollissima 249,000 33 Bivalves Eurasian Oystercatcher Haematopus ostralegus 507,000 50 Bivalves Pied Avocet Recurvirostra avosetta 39,000 53 Polychaetes Common Ringed Plover Charadrius hiaticula 34,300 18 Polychaetes Kentish Plover Charadrius alexandrinus 700 1 Mixed benthos Eurasian Golden Plover Pluvialis apricaria 127,000 17 Polychaetes Grey Plover Pluvialis squatarola 149,000 60 Polychaetes Red Knot Calidris canutus 358,000 100 Bivalves Sanderling Calidris alba 36,800 31 Polychaetes Curlew Sandpiper Calidris ferruginea 13,500 1 Polychaetes Dunlin Calidris alpina 1,154,000 87 Polychaetes Bar-tailed Godwit Limosa lapponica 161,000 100 Polychaetes Eurasian Whimbrel Numenius phaeopus 3900 1 Mixed benthos Eurasian Curlew Numenius arquata 324,000 38 Mixed benthos Spotted Redshank Tringa erythropus 20,500 23 Mixed benthos Common Redshank Tringa totanus 84,400 34 Mixed benthos Common Greenshank Tringa nebularia 26,000 11 Mixed benthos Ruddy Turnstone Arenaria interpres 8500 10 Mixed benthos Black-headed Gull Larus ridibundus 461,000 11 Mixed benthos Common Gull Larus canus 225,000 10 Mixed benthos Herring Gull Larus argentatus 194,000 7 Bivalves 82 M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88 calculated for Common Ringed Plover (Ch. hiaticula hiaticula), Red increases in 6 species (27%) and significant decreases in 16 (73%). On Knot (Calidris canutus islandica), Bar-tailed Godwit (Limosa lap- average, the declines are stronger than the increases but large ponica lapponica), Common Redshank (Tringa totanus robusta) and differences exist between species (Fig. 2, see appendix A for yearly Ruddy Turnstone (population from NE Canada and Greenland). For indices per species). If we relate the population trends to the species’ the other subspecies of these species, no flyway trends are available main diet, we find that 100% of the bivalve specialists have declined (Nagy et al., 2012). Subspecies-specific Wadden Sea trends are since 1991(n ¼ 4), 80% of the species depending on a mixed diet of calculated by basing the yearly indices only on those months in macrobenthos (n ¼ 10) and 50% of the polychaete specialists (n ¼ 8). which these subspecies occur in the Wadden Sea (Meininger et al., To test whether the trends at the Wadden Sea level are site 1995; Wahl et al., 2007; Laursen et al., 2010). Comparison of the specific or part of a broader development we compared the trends flyway and Wadden Sea trends were carried out for the period in the Wadden Sea with the trends on flyway level (based on Nagy 1991/92e2007/08 only, as the counts of January 2009 were not et al., 2012) for 11 species (Fig. 3). Species population trends within available on the flyway level yet. Interactions between trends, the Wadden Sea are significantly more negative than the pop- region and food choice were analysed by calculating region-specific ulation trends in the total flyway (Fig. 3, n ¼ 11, paired t-test, trends and allocating species in three feeding guilds: bivalve t ¼ 4.35, p ¼ 0.001). Seven species with stable or increasing trends feeders (n ¼ 4), polychaete feeders (n ¼ 8) and mixed benthos at the flyway level decrease in the Wadden Sea. In all species except feeders (n ¼ 10). Species were allocated to diets according to Common Shelduck, the decline in the Wadden Sea is stronger or the Leopold et al. (2004) (see Table 1). To assess whether the trends of increase less strong than the flyway trend. the species within the three feeding guilds differed between We also investigated the variability of the trends within the regions, we used repeated measures ANOVA. To assess whether the Wadden Sea itself. Are the trends more or less the same in all regions trends of the species of each feeding guild within each region or tidal basins? The average trends of polychaete specialists differ differed from 1 (no trend), we used a t-test. significantly between regions (repeated measures ANOVA: F ¼ 5.63, Patterns in trends at a smaller spatial scale were investigated by p ¼ 0.01), whereas the average trends of bivalve specialists and calculating trends for each separate tidal basin (Fig. 1), after allo- mixed benthivores do not (F ¼ 1.19, p ¼ 0.37 and F ¼ 2.11, p ¼ 0.12 cating counting units to the nearest tidal basin. When a counting respectively) (Fig. 4). Polychaete specialists show on average nega- unit was located at the border of two tidal basins bird numbers tive trends in Niedersachsen and Schleswig-Holstein, whereas were divided equally between the two different tidal basins. The average trends in the Netherlands and Denmark are positive, though resulting bird numbers per tidal basin were analysed the same way non-significant in Denmark. This pattern resembles the pattern for as described above. Common Eider trends were not analysed this the mixed benthos feeders, although only the average decline in way, as only totals per region were available. The linear trends per Schleswig-Holstein is statistically significant. Bivalve specialists tidal basin were further analysed using Principal Component have declined on average in all regions, except for Denmark where Analysis (PCA; Pielou, 1984). We used PCA (indirect gradient anal- trends of bivalve specialists have been rather diverse. ysis) in CANOCO 4.5 for Windows on the dataset containing 21 The trends at a smaller spatial scale, the individual tidal basins species and 38 tidal basin samples (basins 8 and 9 were merged in (n ¼ 38, Fig. 1), are presented in Fig. 5A and B for polychaete and the shape-files we used). The result is an ordination diagram in which the samples (tidal basins) are displayed by points. The larger Sanderling the distance between the tidal basins in the diagram, the larger the differences in species trends in these samples (Pielou, 1984). Ruddy Turnstone Common Ringed Plover 2.4. Consistency of the monitoring Bar-tailed Godwit Curlew Sandpiper Since 1991 the same boundaries of counting units have been Common Shelduck used, helping to maintain the consistency of the counts. Many of Eurasian Curlew the counting units are counted by the same observers year after Common Greenshank year, which will help in maintaining consistency as well. During Common Redshank counts of waterbirds in tidal areas it is often necessary to count thousands of birds in short periods of time. During these counts Red Knot errors can be made, but errors in counts of individual roosts tend to Common Gull average each other out and results become more accurate when Dunlin based on estimates of many different roosts (Rappoldt et al., 1985), Grey Plover which is the case in current analyses. The errors could increase the Black-headed Gull variation between the yearly indices but are much less likely to Pied Avocet influence the overall trend. The quality of the estimates for missing Eurasian Whimbrel counts can have a bigger influence on the results that we present. Herring Gull On average 49% of the counts is missing and this percentage ranges from 40% in Grey Plover to 56% in Common Gull. Evidence that Eurasian Golden Plover trends with up to 60% missing values can still be accurate comes Eurasian Oystercatcher from simulation studies in which we generated variable amounts of Spotted Redshank missing values (with a realistic pattern of occurrence) in an origi- Common Eider nally complete dataset of monthly counts (Van Roomen et al., 2002; Kentish Plover Soldaat et al., 2004; Atkinson et al., 2006). -8 -6 -4 -2 0 2 4 6 8 3. Results % yearly change

Fig. 2. Population trends of waterbirds depending on the intertidal flats of the Wadden Population declines predominate in waterbird species depend- sea, expressed as the rate of annual change (in % with 95%-confidence limits) over the ing on tidal mudflats in the Wadden Sea since 1991, with significant period 1991e2009. All changes are significant. M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88 83

4 A 5 32 4 3 BtG CG RT 3 2 DK 2 23 1 33 SH CRP CR EC 1 22 4 Du 38 BG CS 5 10 1 RK 11 6 7 39 0 PCA Axis 2 28 9 0 14 24 20 2 34 NS 18 25 29 12 26 30 37 15 17 16 19 36 3 -1 27 21 -1 13 International Flyway 35 NL

-2 -2 31

EO -3 -3 -3 -2 -1 0 1 2 3 PCA Axis 1 -4 -4 -3 -2 -1 0 1 2 3 4 3 Wadden Sea B 35

Fig. 3. The annual rate of change within the Wadden sea (this study) compared with 2 the annual rate of change of the flyway population (from Nagy et al., 2012) for the 34 6 e 33 years 1991 2008. Dots represent species/populations: CS (Common Shelduck), EO 37 (Eurasian Oystercatcher), CRP (Common Ringed Plover, population Ch. hiaticula hia- DK 1 5 18 ticula), RK (Red Knot, population C. canutus islandica), BtG (Bar-tailed Godwit, pop- 38 3 1 7 ulation L. lapponica lapponica), EC (Eurasian Curlew), CR (Common Redshank, 39 4 36 population T. totanus robusta), RT (Ruddy Turnstone, breeding population from NE 11 12 10 2 SH Canada and Greenland), BG (Black-headed Gull) and CG (Common Gull). For the other 0 9 19 22 30 15 14 21 fl 13 subspecies of the wader species mentioned no yway trends were available. 16 17 32 PCA Axis 2 23 29 NS 31 20 bivalve specialists respectively. In polychaete feeders, the pattern -1 27 28 26 observed at the regional level is also more or less visible at a smaller spatial scale, with Niedersachsen (nrs 19e29) and Schleswig- 25 NL Holstein (nrs 5e18) forming a distinct group, separated from -2 Denmark (nr 1e4) and The Netherlands (nr 30e39) (Fig. 5A). The 24 PCA plot for the three bivalve specialists (Common Eider could not be included) shows the tidal basins of the western Dutch Wadden -3 Sea (nr 37e39) forming a group together with the tidal basins in -3 -2 -1 0 1 2 3 PCA Axis 1 Schleswig-Holstein (nr 5e18), whereas the tidal basins of most of the eastern Dutch Wadden Sea (nr 30e36) are more comparable Fig. 5. PCA diagrams, showing the position of the different tidal basins along the two with tidal basins in Denmark (nr 1e4). The tidal basins of major axes, for (A) polychaete feeding waterbirds and (B) bivalve feeding waterbirds. Niedersachsen (nr 19e29) and the two Dutch tidal basins close to Eigenvalues of axis 1 and 2 are 0.57 and 0.17 in (A) and 0.92 and 0.06 in (B). Tidal basins are marked by different symbols as located within Denmark, Schleswig-Holstein, Niedersachsen geographically (nr 31e32) take an intermediate Niedersachsen and The Netherlands. Numbers refer to Fig. 1. position (Fig. 5B).

10 4. Discussion

The Wadden Sea is famous for its importance for migratory P= 0.37 P= 0.01 P= 0.12 5 waterbirds. Among them, the specialists of intertidal mudflats form a dominant group. It is therefore alarming that a majority (73%) of NL NS these species have declined since 1991. If we look at the total time 0 SH period for which we have Wadden Sea trends for all regions DK together, from 1987 onwards, 59% of the 22 selected species are in

% yearly change -5 decline or have a declining tendency (JMMB, 2010). In some species the developments are not linear and in a minority different periods of trend directions can be distinguished but this does not alter the -10 conclusion that many species are in decline (Appendix A). This bivalves (4) polychaetes (8) mixed benthos (10) situation conflicts with the targets of the Wadden Sea Plan, aiming main diet at stable or increasing population numbers. The Wadden Sea Plan Fig. 4. Trends of waterbirds depending on the intertidal flats of the Wadden sea, bird targets are also representative for the Natura 2000 objectives averaged per region and per feeding guild (including 95%-confidence limits). Number and the World Heritage site criteria. of species per feeding guild is given in brackets. P-values in the figure refer to signif- It is therefore important to try to find the drivers behind these icance of differences in trends per feeding guild between regions (repeated measures ANOVA), asterisks refer to significant trends of feeding guilds per region (t-test: declines. Monitoring projects can signal developments of concern ***P < 0.001, **P < 0.01, *P < 0.05). but are generally not able to illuminate directly the causes behind 84 M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88 them. However, they can help in narrowing down the number of these areas (Maclean et al., 2008). For the Wadden Sea it has possibilities and point in the direction of likely hypotheses. The already been shown that more birds remain to winter in the eastern waterbird species analysed in this paper are migratory and most part during mild winters and that they may also depart earlier to populations are present in the Wadden Sea for parts of the year only. their northern breeding grounds when springs are warm (Bairlein Changes in numbers may reflect factors impacting on these pop- and Exo, 2007). However, on the basis of this hypothesis, we ulations in other parts of the flyway, factors impacting in the whole would expect a shift in distribution from the warmer parts of the flyway or factors operating in the Wadden Sea only. It is therefore an Wadden Sea to the colder parts, not an increase in the warmer part important step if we can narrow down the number of possibilities. (The Netherlands), a decrease in a colder part (Germany) and an We investigated both the trends for the same populations in increase again in the coldest part (Denmark), as we observed, relation to a larger spatial scale (i.e. the whole flyway) and smaller especially in polychaete specialists. Besides positive effects on spatial scales (i.e. regions and tidal basins within the Wadden Sea). feeding conditions for waterbirds, climate warming could also At the flyway level, some important populations could not be negatively affect stocks of bivalves (Beukema and Dekker, 2005). analysed, as flyway trends were lacking for these (Nagy et al., 2012). However also then one would expect a gradual pattern from the This is the case particularly for populations utilising the Wadden warmer southwest towards the colder northeast and not the Sea on passage to and from wintering areas in West Africa (i.e. the present pattern of decreasing trends of bivalve eaters in the populations canutus for Knot and taymyrensis for Bar-tailed western Dutch Wadden Sea and Germany and increases in the Godwit). We could however analyse trends for most populations eastern Dutch Wadden Sea and Denmark. Despite changing trends wintering in Western Europe and the western Mediterranean, across NW-Europe mediated by global change, the mechanisms of excluding Common Eider and Herring Gull however (Nagy et al., improved wintering conditions or lower stocks of bivalves cannot 2012). For the selection of species, trends in the Wadden Sea explain the more detailed pattern in trends within the Wadden Sea. were more negative than the trend of these flyway populations as However, climate change could also have effects in other ways. a whole. This suggests that causes for the Wadden Sea trends needs Laursen et al. (2010) draw attention to the fact that the Wadden Sea to be sought within the Wadden Sea itself. This notion gets further regions where negative trends dominate are characterized by support from the large differences in population trends between a large tidal amplitude, whereas areas where bird numbers have regions and tidal basins within the Wadden Sea itself. It is unlikely generally increased are characterized by a small tidal amplitude. that factors outside the Wadden Sea or operating along the whole Large tidal amplitudes occur in the centre of the German Bight, flyway will have such diverse effects within the Wadden Sea covering Schleswig-Holstein and parts of Niedersachsen, and without specific factors operating within the Wadden Sea itself. smaller amplitudes occur in The Netherlands and Denmark. The Earlier studies have already concentrated on possible causes central Wadden Sea is also more exposed because of the lack of behind the many decreasing trends in the Wadden Sea (Reineking larger barrier islands (see Fig. 1). Laursen et al. (2010) hypothesize and Südbeck, 2007) and the differences in trends between Wadden that the observed changes in wind direction, sea level and Sea regions (Ens et al., 2009a). Many of the hypotheses (involving temperature (Oost et al., 2009; Philippart and Epping, 2009) could 20 different drivers) listed by Ens et al. (2009a) might apply, but affect the central Wadden Sea most with for instance effects on insufficient data limited powerful correlative analysis to further sediment composition. A coarsening of the sediment due to narrow down the possibilities. However, the data assembled in that increased hydrodynamical forces is likely to reduce the stocks of study and in Marencic and De Vlas (2009) indicate that eutrophi- benthic invertebrates (Dolch and Reise, 2009). This is an important cation, climate change, shellfish fisheries, tourism, and changes in hypothesis to investigate further. biological communities are the most important drivers to be Evidence of strong ecological effects of shellfish fisheries on investigated further. We have to find a driver (or a combination of tidal mudflats in the Wadden Sea has accumulated (Ens et al., 2004; drivers) which explains decreasing trends of polychaete specialists Piersma et al., 2001). As a result, the numbers of Eurasian Oyster- in Germany and increases in Denmark and the Netherlands and catcher (Ens, 2006; Rappoldt et al., 2003) and Red Knot (Van Gils decreasing trends of bivalve specialists in the western Dutch et al., 2006) decreased in the Dutch Wadden Sea. It has been sug- Wadden Sea and Schleswig-Holstein and increases in Denmark and gested that the other side of the coin could be increasing numbers partly in the eastern Dutch Wadden Sea. of polychaete specialists (Van Roomen et al., 2005). Some evidence Since the 1980s the input of nutrients (phosphorus and nitrogen) exists that polychaetes increase in sediments disturbed by cockle into the Wadden Sea has declined, which correlates with lower dredging (Kraan et al., 2007). Also in the Wash in England, a similar phytoplankton biomass (Van Beusekom et al., 2009). Time series difference in response between shellfi sh and polychaete specialists analysis (Philippart et al., 2007) and model calculations (Brinkman was found, related to fisheries and also nutrient input (Atkinson and Smaal, 2004) for the western Dutch Wadden Sea indicated et al., 2010). The difference in trends between the western and that stocks of filter feeding bivalves have declined as a result. This fits eastern Dutch Wadden Sea also seems related to differential fairly well with the observed decline in shell fish-eaters in the intensity of fishing and conservation measures afterwards (Ens western Dutch Wadden Sea. Furthermore, higher phytoplankton et al., 2009b). However, the Eurasian Oystercatcher did not levels are found in Denmark and the eastern Dutch Wadden Sea increase in the eastern Dutch Wadden Sea. In general, fishing (Van Beusekom et al., 2009), which are the regions with positive intensity seems to have been much more intense in the trends for bivalve eaters at present. However, also around the Elbe Netherlands than in the other Wadden Sea regions (Nehls et al., relatively high phytoplankton levels are present and there declines 2009b). Consequently, if fishing intensity would be the dominant of bivalve eaters predominate. Hence, eutrophication seems to play driver, in general positive or less negative trends for bivalve eaters a role but is not able to explain the whole picture. would be expected in Germany and Denmark than in The Climate change may impact on the populations of waterbirds in Netherlands, which is clearly not the case in Germany. In addition, different ways. Higher temperatures decrease energy expenditure it does not seem very likely that the strongly decreasing trends in of warm-blooded animals like birds. Moreover, when mudflats are polychaete specialists in Germany are caused by the continued less likely to freeze this will have positive affects on the feeding absence of mudflat dredging fisheries. Despite clear relations at conditions during winter. A recent analysis of wader populations a regional level, the extrapolation of the effects of fisheries towards wintering in Europe indicated a shift in distribution to the north- the whole Wadden Sea is problematic and fisheries alone seem not east during the last 30 years, in line with milder temperatures in to be able to explain the overall patterns observed. M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88 85

The Wadden Sea is a very important area for tourism and et al. (2009a) made clear that reliable data on explanatory vari- recreation (Brandt and Wollesen, 2009) and disturbance of roosting ables are scarce and sampling scales and periods differ between and feeding sites can have strong impacts on waterbird numbers Wadden Sea regions. Testing the hypotheses requires an improved (Madsen, 1998; Koffijberg et al., 2003). However the general level of monitoring of the explanatory variables at a spatial and temporal protection and conservation measures within the Wadden Sea is scale comparable to the scales of the bird monitoring program. rather high and it seems unlikely that disturbance can explain the Making the Wadden Sea into a Long-Term Ecological Research Site different patterns in trends observed (Madsen, 2007). would greatly help this enterprise (Van Beusekom et al., 2010). As As food is the dominant factor influencing bird numbers, changes most of the decreases are presently found in Germany it seems in the available macrofauna for waterbirds through invasive alien important that thorough studies will be started there, in addition to species can have a large influence (Nehring et al., 2009). Important others in the Netherlands and Denmark. More fundamental recent invaders to consider in this respect are PacificoystersCras- knowledge is needed about the population dynamic processes sostrea gigas (Nehls et al., 2006), the American razor clam Ensis (reproduction and survival) in relation to habitat use to really directus (Tulp et al., 2010; Van de Graaf et al., 2009) and polychaetes understand the changes in the Wadden Sea and its effects on birds like Marenzelleria viridis (Van de Graaf et al., 2009). However, (Greenwood et al., 1993; Reneerkens et al., 2005; Van der Jeugd although important changes due to these new invaders will take et al., 2008; van de Pol et al., 2010a,b). Furthermore, it is essential place, it seems unlikely that these will correlate with the region- and/ that more information becomes available from other sites in the or tidal basin-specific trends observed. Another change in biological flyway, since in the course of a year Wadden Sea bird species use community to consider is the increasing numbers of Peregrine areas as diverse and distant as the high Arctic and the western Falcons (Falco peregrinus) within the Wadden Sea as potential seaboard of Africa. Only a combination of monitoring within the predators of especially waders. It is not the increase in actual Wadden Sea and within the East-Atlantic Flyway will help in mortality, which would be important, but the perceived increase in understanding the many threats to migratory waterbirds. predation risk, which will result in lower numbers (Ydenberg et al., 2007; Van den Hout, 2009). An overview of the potential predation Acknowledgements pressure on waders across the Wadden Sea is lacking but this will be an interesting exercise. Numbers of breeding Peregrines Falcons are First of all we like to acknowledge the hard and dedicated work of higher in the German than in the Dutch and Danish Wadden Sea and the observers carrying out the counts. We also like to thank Eelke this could have an effect particularly in the early autumn and late Folmer and Folkert de Jong for making available the shape-files of the spring periods in which the largest decreases in numbers of waders tidal basins to us. Szabolcs Nagy, Tom Langendoen and Stephan Flink are observed in Germany (Leyrer, 2011; Laursen et al., 2010). from Wetlands International allowed us to use the flyway trends. Altogether we have found some promising hypotheses, but Hans Schekkerman advised on statistics and commented on the cannot yet fully explain the patterns we observed. This is in a way manuscript. Comments from three anonymous referees improved disappointing as the declines have been ongoing for a relatively long the paper substantially. This paper is written with financial support time and we are still not able to advise on specific management from the Rob Goldbach publication fund through SOVON. measures needed to stop them. On the one hand the comparisons made are still on a coarse scale and more advanced analyses are Appendix A. Yearly indices per species in the Wadden Sea needed to test the hypotheses, on the other hand it is likely that 1991/92e2008/09. Numbers on the y-axes are the average more drivers are operating at the same time and in interaction with number in the Wadden Sea over 12 months periods from each other, complicating the analyses. Further studies are needed to JulyeJune. The line is the trend as calculated by log-linear test current hypotheses including testing of multiple factors Poisson regression. working simultaneously. This will not be easy as the study of Ens

Common Shelduck Common Eider Eurasian Oystercatcher 160,000 350,000 500,000

140,000 300,000 400,000 rebmunegareva re 120,000 rebm 250,000 bmun 100,000 300,000 200,000 un 80,000 eg egar 150,000 60,000 areva 200,000 e 100,000 va 40,000 100,000 20,000 50,000

0 0 0 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 season season season

Pied Avocet Common Ringed Plover Kentish Plover 25,000 10,000 400

20,000 8,000 rebm rebmunegareva rebm 300

15,000 6,000 un un 200 egar egare 10,000 4,000 eva va 100 5,000 2,000

0 0 0 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 season season season 86 M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88

Eurasian Golden Plover Grey Plover Red Knot 100,000 80,000 300,000

250,000 80,000 reb r rebmunegareva 60,000 ebmunega 200,000

60,000 munega 40,000 150,000 40,000 re re 100,000 va va 20,000 20,000 50,000

0 0 0 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 season season season

Sanderling Curlew Sandpiper Dunlin 16,000 4,000 800,000

14,000 r r 12,000 r 3,000 600,000 eb ebmunegareva e b m 10,000 mun unegar 8,000 2,000 400,000 eg

6,000 areva e va 4,000 1,000 200,000

2,000

0 0 0 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 season season season

Bar-tailed Godwit Eurasian Whimbrel Eurasian Curlew 120,000 1,200 250,000

100,000 1,000 200,000 re re re bmun b bmu 80,000 800

muneg 150,000 neg 60,000 600 eg a a a 100,000 reva reva reva 40,000 400

50,000 20,000 200

0 0 0 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 season season season

Spotted Redshank Common Redshank Common Greenshank 8,000 40,000 7,000

6,000 r reb re 6,000 30,000

eb 5,000 b mune munega mune 4,000 4,000 20,000 gare ga 3,000 rev re v v a a a 2,000 2,000 10,000 1,000

0 0 0 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 season season season

Ruddy Turnstone Black-headed Gull Common Gull 7,000 200,000 120,000

6,000 100,000 reb reb rebmunegarev 150,000 5,000 80,000 mun 4,000 mun 100,000 60,000 ega ega 3,000 rev rev 40,000 a a a 2,000 50,000 1,000 20,000

0 0 0 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 1991 1993 1995 1997 1999 2001 2003 2005 2007 season season season

Herring Gull 200,000

rebmuneg 150,000

100,000 a r eva 50,000

0 1991 1993 1995 1997 1999 2001 2003 2005 2007 season M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88 87

References 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 Atkinson, P.W., Austin, G.E., Rehfisch, M.M., Baker, H., Cranswick, P., Kershaw, M., schelpdiervisserij tweede fase). Deelproject C2. Alterra Rapport 954, 1e165. Robinson, J., Langston, R.H.W., Stroud, D.A., van Turnhout, C., Maclean, I.M.D., SOVON-onderzoeksrapport 2004/07. 2006. Identifying declines in waterbirds: the effects of missing data, population Leyrer J., 2011. Being at the right time at the right place: interpreting the annual life variability and count period on the interpretation of long-term survey data. cycle of Afro-Siberian red knots. PhD thesis, University of Groningen, Gronin- Biological Conservation 130, 549e559. gen, The Netherlands. Atkinson, P.W., Maclean, I.M., Clark, N.A., 2010. Impacts of shellfisheries and Maclean, I.M.D., Austin, G.E., Rehfisch, M.M., Blew, J., Crowe, O., Delany, S., Devos, K., nutrient inputs on waterbird communities in the Wash, England. Journal of Deceuninck, B., Gunther, K., Laursen, K., Van Roomen, M., Wahl, J., 2008. Climate Applied Ecology 47, 191e199. change causes rapid changes in the distribution and site abundance of birds in Bairlein, F., Exo, K.M., 2007. Climate change and migratory waterbirds in the winter. Global Change Biology 14, 2489e2500. Wadden Sea. In: Reineking, B., Südbeck, P. (Eds.), Seriously Declining Trends in Madsen, J., 1998. Experimental refuges for migratory waterfowl in Danish wetlands. Migratory Waterbirds: Causes-Concerns-Consequences. Wadden Sea I. Baseline assessment of the disturbance effects of recreational activities. Ecosystem, vol. 23. Common Wadden Sea Secretariat, Wilhelmshaven. Journal of Applied Ecology 35, 386e397. Germany, pp. 43e52. Madsen, J., 2007. Possible effects and impacts of recreational activities on bird Bell, M.C., 1995. UNIDEX4. A Computer Programme for Estimating Population Index populations in the wadden sea - Can disturbance explain the negative trends? Numbers by the Underhill Method. The Wildfowl and Wetlands Trust, Slim- In: Reineking, B., Südbeck, P. (Eds.), Seriously Declining Trends in Migratory bridge, UK, P. 9. Waterbirds: Causes-Concerns-Consequences. Common Wadden Sea Secretariat, Beukema, J.J., Dekker, R., 2005. Decline of recruitment success of cockles and other Wilhelmshaven, pp. 65e68. bivalves in the Dutch Wadden Sea: possible role of climate change, predation Marencic, H., De Vlas, J. (Eds.), 2009. Quality status Report 2009. Wadden Sea on postlarvae and fisheries. Marine Ecology Progress Series 287, 149e167. ecosystem, vol. 25. Common Wadden Sea Secretariat, Trilateral Monitoring and Blew, J., Günther, K., Laursen, K., van Roomen, M., Südbeck, P., Eskildsen, K., Potel, P., Assessment Group, Wilhelmshaven, Germany. 2007. Trends of waterbird populations in the international wadden Sea 1987e2004: an update. In: Reineking, B., Südbeck, P. (Eds.), Seriously Declining Meininger, P.L., Schekkerman, H., Van Roomen, M.W.J., 1995. Populatieschattingen en 1 procent-normen van in Nederland voorkomende watervogelsoorten: Trends in Migratory Waterbirds: Causes e Concerns e Consequences. Wadden voorstellen voor standaardisatie. Limosa 68, 41e48. Sea Ecosystem, vol. 23. Common Wadden Sea Secretariat, Wilhelmshaven, Meltofte, H., Blew, J., Frikke, J., Rosner, H.U., Smit, C.J., 1994. Numbers and distri- Germany, pp. 9e32. bution of waterbirds in the Wadden Sea; results and evaluation of 36 simul- Brandt, A.C., Wollesen, A., 2009. Tourism and Recreation. Thematic Report No. 3.4. taneous counts in the Dutch-German-Danish Wadden Sea 1980e1991. IWRB In: Marencic, H., De Vlas, J. de (Eds), 2009. Quality Status Report 2009. Wadden Publication vol. 34. Wader Study Group Bulletin vol. 74 (Special Issue), 1e192. Sea Ecosystem No. 25. Common Wadden Sea Secretariat, Trilateral Monitoring Denmark; CWSS, IWRB, Wader Study Group. and Assessment Group, Wilhelmshaven, Germany. Nagy, S., Flink, S., Langendoen, T., Delany, S., 2012. Report on the Conservation Brinkman, A.G., Smaal, A.C., 2004. Onttrekking en natuurlijke productie van Status of Migratory Waterbirds in the Agreement Area of the African-Eurasian schelpdieren in de Nederlandse Waddenzee in de periode 1976e1999. Alterra Waterbird Agreement. Wetlands International, Wageningen. Rapport 888, 1e243. Nehls, G., Diederich, S., Thieltges, D.W., Strasser, M., 2006. Wadden Sea mussel beds Dolch, T., Reise, K., 2009. Long-term displacement of intertidal seagrass and mussel invaded by oysters and slipper limpets: competition or climate control? Hel- beds by expanding large sandy bedforms in the northern Wadden Sea. Journal goland Marine Research 60, 135e143. of Sea Research. doi:10.1016/j.seares.2009.10.004. Nehls, G., Witte, S., Büttger, H., Dankers, N., Jansen, J., Millat, G., Herlyn, M., Ens, B.J., 2006. The conflict between shellfisheries and migratory waterbirds in the Markert, A., Kristensen, P.S., Ruth, M., Buschbaum, C., Wehrmann, A., 2009a. Dutch Wadden Sea. In: Boere, G.C., Galbraith, C.A., Stroud, D.A. (Eds.), Water- Beds of blue mussels and Pacific oysters. In: Marencic, H., De Vlas, J. (Eds.), birds Around the World. The Stationery Office, Edinburgh, UK, pp. 806e811. 2009a. Quality Status Report 2009. Wadden Sea Ecosystem, vol. 25. Common Ens, B.J., Smaal, A.C., De Vlas, J., 2004. The effects of shellfish fishery on the Wadden Sea Secretariat, Trilateral Monitoring and Assessment Group, Wil- ecosystems of the Dutch Wadden Sea and Oosterschelde. Final report on the helmshaven, Germany. second phase of the scientific evaluation of the Dutch shellfish fishery policy Nehls, G., Witte, S., Dankers, N., de Vlas, J., Quirijns, F., Kristensen, P.S., 2009b. (EVA II). Alterra-rapport 1011; RIVO-rapport C056/04; RIKZ-rapport RKZ/ Fishery. Thematic Report No. 3.3. In: Marencic, H., De Vlas, J. (Eds.), 2009b. 2004.031, 1e212. Wageningen, Alterra. Quality Status Report 2009. Wadden Sea Ecosystem, vol. 25. Common Wadden Ens, B., Blew, J., Van Roomen, M., van Turnhout, C., 2009a. Exploring contrasting Sea Secretariat, Trilateral Monitoring and Assessment Group, Wilhelmshaven, trends of migratory waterbirds in the Wadden Sea. In: Wadden Sea Ecosystem, Germany. vol. 27. Common Wadden Sea Secretariat, Wilhelmshaven. Germany, p. 27. Nehring, S., Reise, K., Dankers, N., Kristensen, P.S., 2009. Alien species. In: Ens, B.J., Van Winden, E.A.J., Van Turnhout, C.A.M., van Roomen, M.W.J., Smit, C.J., Marencic, H., De Vlas, J. (Eds.), Thematic Report No. 7. Quality Status Report Jansen, J.M., 2009b. Changes in the abundance of intertidal birds in the Dutch 2009. WaddenSea Ecosystem, vol. 25. Common Wadden Sea Secretariat, Wadden Sea in 1990e2008: differences between east and west. Limosa 82,100e112. Trilateral Monitoring and Assessment Group, Wilhelmshaven, Germany. Eriksson, B.K., Van der Heide, T., van de Koppel, J., Piersma, T., Van der Veer, H.W., Oost, A., Kabat, P., Wiersma, A., Hofstede, J., 2009. Climate. In: Marencic, H., De Olff, H., 2010. Major changes in the ecology of the Wadden sea: human impacts, Vlas, J. (Eds.), Thematic Report No. 4.1. Quality Status Report 2009. Wadden Sea ecosystem engineering and sediment dynamics. Ecosystems 13, 752e764. Ecosystem, vol. 25. Common Wadden Sea Secretariat, Trilateral Monitoring and Furness, R.W., Greenwood, J.J.D., 1993. Birds as Monitors of Environmental Change. Assessment Group, Wilhelmshaven, Germany. Chapman & Hall, London. Pannekoek, J., van Strien, A., 2001. TRIM 3 Manual (TRends & indices for monitoring Greenwood, J.J.D., Baillie, S.R., Crick, H.Q.P., Marchant, J.H., Peach, W.J., 1993. Inte- data), CBS Research Paper No. 0102: pp. 1e57. grated population monitoring: detecting the effects of diverse changes. In: Philippart, K., Epping, E., 2009. Climate change and ecology. Thematic Report No. Furness, R.W., Greenwood, J.J.D. (Eds.), Birds as Monitors of Environmental 4.2. In: Marencic, H., De Vlas, J. (Eds.), 2009. Quality Status Report 2009. Change. Chapman & Hall, London, pp. 267e342. Wadden Sea Ecosystem, vol. 25. Common Wadden Sea Secretariat, Trilateral JMMB, 2010. Trends of Migratory and Wintering Waterbirds in the Wadden Sea Monitoring and Assessment Group, Wilhelmshaven, Germany. 1987/88-2008/09 (Wilhelmshaven Germany). www.waddensea-secretariat.org. Philippart, C.J.M., Beukema, J.J., Cadée, G.C., Dekker, R., Goedhart, P.W., Van Koffijberg, K., Blew, J., Eskildsen, K., Günther, C., Koks, B., Laursen, K., Rasmussen, Iperen, J.M., Leopold, M.F., Herman, P.M.J., 2007. Impacts of nutrient reduction L.M., Potel, P., Sudbeck, P., 2003. High tide roosts in the Wadden Sea: A review of on coastal communities. Ecosystems 10, 96e119. bird distribution, protection regimes and potential sources of anthropogenic Pielou, E.C., 1984. The Interpretation of Ecological Data. Wiley, New York. disturbance. Wadden Sea Ecosystem No. 16, 1e120. Wilhelmshaven, Common Piersma, T., Koolhaas, A., 1997. Shorebirds, Shellfish(eries) and Sediments Around Wadden Sea Secretariat, Trilateral Monitoring and Assessment Group, Joint Griend, Western Wadden Sea, 1988e1996. NIOZ-Rapport 1997-7, 1e118. Den Monitoring Group of Migratory Birds in the Wadden Sea. Burg, NIOZ. Kraan, C., Piersma, T., Dekinga, A., Koolhaas, A., Van der Meer, J., 2007. Dredging for Piersma, T., Koolhaas, A., Dekinga, A., Beukema, J.J., Dekker, R., Essink, K., 2001. edible cockles (Cerastoderma edule) on intertidal flats: short-term consequences Long-term indirect effects of mechanical cockle-dredging on intertidal bivalve of fisher patch-choice decisions for target and non-target benthic fauna. ICES stocks in the Wadden Sea. Journal of Applied Ecology 38, 976e990. Journal of Marine Science 64, 1735e1742. Rappoldt, C., Kersten, M., Smit, C.J., 1985. Errors in large scale shorebird counts. Kraft, D., Folmer, E., Meyerdirks, J., Stiehl, T., 2011. Data Inventory of Tidal Basins in Ardea 73, 13e24. the Trilateral Wadden Sea. Common Wadden Sea Secretariat, Wilhelmshaven, Rappoldt, C., Ens, B.J., Dijkman, E., Bult, T., 2003. Scholeksters en hun voedsel in de Germany. Waddenzee. Rapport voor deelproject B1 van EVA II, de tweede fase van het Kristensen, P.S., Borgstrøm, R., 2006. The Danish Wadden Sea; fishery of mussels evaluatieonderzoek naar de effecten van schelpdiervisserij op natuurwaarden (Mytilus edulis L.) in a Wildlife Reserve? In: Laursen, K., (Ed.), Monitoring and in de Waddenzee en Oosterschelde 1999e2003. Alterra Rapport 882, 1e152. Assessment in the Wadden Sea. Proceedings from the 11. Scientific Wadden Sea Wageningen, Alterra. Symposium, Esbjerg, Denmark, 4e8. April, 2005. NERI Technical Report No. 573, Reineking, B., Südbeck, P., 2007. Seriously declining trends in migratory waterbirds: pp. 113e122. causes-concerns-consequences. In: Proceedings of the International Workshop Laursen, K., Blew, J., Eskildsen, K., Gunther, K., Halterlein, B., Kleefstra, R., on 31 August 2006 in Wilhelmshaven, Germany. Wadden Sea Ecosystem, vol. Luersen, G., Potel, P., Schrader, S., 2010. Migratory waterbirds in the Wadden Sea 23. Common Wadden Sea Secretariat, Wadden Sea National Park of Lower 1987e2008. In: Wadden Sea Ecosystem, vol. 30. Common Wadden Sea Secre- Saxony, Institute of Avian Research, Wilhelmshaven, Germany, pp. 1e75. tariat, Wilhelmshaven, Germany, pp. 1e170. 88 M. van Roomen et al. / Ocean & Coastal Management 68 (2012) 79e88

Reneerkens, J., Piersma, T., Spaans, B., 2005 De Waddenzee als kruispunt van frequency, magnitude and timing of extreme climatic events threaten the vogeltrekwegen. NIOZ-rapport 2005-4, 1e125. Den Burg, Koninklijk Nederlands population viability of coastal birds? Journal of Applied Ecology 47, 720e730. Instituut voor Onderzoek der Zee (NIOZ). van de Pol, M., Vindenes, Y., Sæther, B.-E., Engen, S., Ens, B.J., Oosterbeek, K., Rösner, H.U., 1993. The Joint Monitoring Project for Migratory Birds in the Wadden Tinbergen, J.M., 2010b. Effects of climate change and variability on population Sea. Common Wadden Sea Secretariat, Wilhelmshaven, Germany, p. 16. dynamics in a long-lived shorebird. Ecology 91, 1192e1204. Smit, C.J., Wolff, W.J., 1981. Birds of the Wadden Sea. Balkema, Rotterdam. Van den Hout, P., 2009. Mortality is the tip of an iceberg of fear; Peregrines Falco Soldaat, L., van Winden, E., van Turnhout, C., Berrevoets, C.M., Van Roomen, M., Van peregrinus and shorebirds in the Wadden Sea. Limosa 82, 122e133. Strien, A., 2004. De berekening van indexen en trends bij het watervogelmeetnet. Van der Jeugd, H.P., Schekkerman, H., Ens, B.J., 2008. Towards integrated pop- SOVON-onderzoeksrapport 2004/02, 1e100. Voorburg/Heerlen, CBS. ulation monitoring of birds in the Wadden sea. Vogeltrekstation Publication, Tulp, I., Craeymeersch, J., Leopold, M., van Damme, C., Fey, F., Verdaat, H., 2010. The p. 1e25. role of the invasive bivalve Ensis directus as food source for fish and birds in the Van Gils, J.A., Piersma, T., Dekinga, A., Spaans, B., Kraan, C., 2006. Shellfish dredging Dutch coastal zone. Estuarine Coastal and Shelf Science 90, 116e128. pushes a flexible avian top predator out of a marine protected area. PLoS Underhill, L.G., Prys-Jones, R., 1994. Index numbers for waterbird populations. I. Biology 4, e376. Review and methodology. Journal of Applied Ecology 31, 463e480. Van Roomen, M., van Turnhout, C., Nienhuis, J., Willems, F., van Winden, E., 2002. Van Beusekom, J.E.E., Bot, P.V.M., Carstensen, J., Goebel, J.H.M., Lenhart, H., Pätsch, J., Monitoring van watervogels als niet-broedvogel in de Nederlanse Waddenzee: Petenati, T., Raabe, T., Reise, K., Wetsteijn, B., 2009. Eutrophication. In: evaluatie huidige opzet en voorstellen voor de toekomst. SOVON-onderzoeks- Marencic, H., De Vlas, J. (Eds.), Thematic Report No. 6. Quality Status Report rapport 2002/01, 1e58. Beek-Ubbergen, SOVON Vogelonderzoek Nederland. 2009. Wadden Sea Ecosystem, vol. 25. Common Wadden Sea Secretariat, Van Roomen, M., van Turnhout, C., van Winden, E., Koks, B., Goedhart, P.W., Trilateral Monitoring and Assessment Group, Wilhelmshaven, Germany. Leopold, M.F., Smit, C.J., 2005. Trends van benthivore watervogels in de Van Beusekom, J.E.E., Buschbaum, C., Loebl, M., Martens, P., Reise, K., 2010. Long-term Nederlandse Waddenzee 1975e2002: grote verschillen tussen schelpdier- ecological change in the northern Wadden sea. In: Müller, F., Baessler, C., eneters en wormeneters. Limosa 78, 21e38. Schubert, H., Klotz, S. (Eds.), Long-Term Ecological Research. Springer, pp.145e153. Wahl, J., Garthe, S., Heinicke, T., Knief, W., Petersen, B., Sudfeldt, C., Südbeck, P., Van de Graaf, S., de Vlas, J., Herlyn, M., Voss, J., Heyer, K., Drent, J., 2009. Macro- 2007. Anwendung des internationalen 1% Kriteriums für wandernde Wasser- zoobenthos. In: Marencic, H., De Vlas, J. (Eds.), 2009. Quality Status Report 2009. vogelarten in Deutschland. Berichte zum Vogelschutz 44, 83e105. Wadden Sea Ecosystem, vol. 25. Common Wadden Sea Secratariat, Trilateral Wetlands International, 2006. Waterbird Population Estimates, fourth ed. Wetlands Monitoring and Assessment Group, Wilhelmshaven, Germany, pp. 1e28. International, Wageningen, The Netherlands, P. 239. Van de Kam, J., Ens, B., Piersma, T., Zwarts, L., 2004. Shorebirds, an Illustrated Ydenberg, R.C., Butler, R.W., Lank, D.B., 2007. Effects of predator landscapes on the Behavioural Ecology. KNNV Publishers, Utrecht, The Netherlands. evolutionary ecology of routing, timing and molt by long-distance migrants. van de Pol, M., Ens, B.J., Heg, D., Brouwer, L., Krol, J., Maier, M., Exo, K.M., Journal of Avian Biology 38 (523529), 2007. doi:10.1111/j.2007.0908- Oosterbeek, K., Lok, T., Eising, C.M., Koffijberg, K., 2010a. Do changes in the 8857.04202.x.