r- Biologie/Chemie, P.O. Box 4469, D-4500 Osnabriick, Germany. FUNCTIONAL AND NUMERICAL RESPONSE OF

441 FUNCTIONAL AND NUMRICAL RSPONS OF OYSTRCATCHRS HAMATOPUS OSTRALGUS ON SHLLFISH POPULATIONS BRUNO J. NS 1, THOMAS MRCK2, COR J. SMITI & ARlO (.) J. BUNSKOKI ns RI., T. Merck, C.I. Smit &.I. Bunskoeke 1996. Functional and numerical response of Oystercatchers Haematopus ostralegus on shellfish populations. Ardea 84A: 441-452. On a mudflat containing five potential prey species, Oystercatchers predominantly took Cockles and Mussels, probably because the densities and the availability of the alternative prey, Baltic Tellin, Ragworm and Shorecrab, were low. The intake rate ofoystercatchers feeding on the mussel bed decreased as water levels dropped and the number of Oystercatchers feeding on the mussel bed declined as more of the adjoining mudflats became exposed. The intake rate of Oystercatchers feeding on Cockles showed a clear positive correlation with the size of the Cockles present, while an effect of the density of the Cockles could not be demonstrated. No evidence was found for interference, i.e. a decrease in intake rate as a result ofan increase in bird density. Since the size of Cockles increased downshore, the intake rate ofoystercatchers feeding on Cockles increased when water levels dropped and the birds moved downshore. IfOystercatchers followed the predictions of the most simple ideal free distribution model, they should have all moved to feeding oncockles when sites below 60 cm NAPuncovered. Though the majority ofbirds behaved according to predictions, a substantial minority continued to feed on the mussel bed during low tide. This is probably due to individual differences in feeding specialization and. perhaps, local dominance. Key words: Oystercatcher - Haematopus ostralegus - ideal free distribution - prey choice - tidal cycle - Cockle - Cerastoderma edule - Mussel - Myti Ius edulis linstitute for Forestry and Nature Research (IBN-DLO), P.O. Box 167, 1790 AD Den Burg, The Netherlands; 2Universitiit Osnabriick, Fachbereich r- Biologie/Chemie, P.O. Box 4469, D-4500 Osnabriick, Germany. INTRODUCTION This paper describes how Oystercatchers Haematopus ostralegus distribute themselves over a habitat that is spatially heterogeneous with respect to the species and sizes of prey available and temporally variable with respect to the areas exposed due to the tide. At each moment in time we can ask where the birds should feed and what prey they should take (see e.g. Stephens & Krebs 1986). Since the two most important prey species were spatially separated in our study area, it was impossible to separate the problem ofprey choice from the problem of site choice when birds switched prey. In contrast, when birds switched site without switching prey, pure, site choice could be studied. Individual Oystercatchers may suffer from interference, i.e. experience a reduction in intake rate, when feeding close to other Oystercatchers (ns & Cayford 1996). As a result, the decision on where to feed is expected to depend on the opposing tendencies to congregate where food is abundant but to avoid other birds (Goss-Custard 1980, Goss-Custard et af. 1996). From the assumptions that animals choosing a territory (1) aim to max-

442 ARDA 84A, 1996 irnize fitness, (2) are ideal (i.e. have perfect knowledge) and (3) are free (i.e. pay no fitness cost for moving) Fretwell & Lucas (1970) and Fretwell (1972) derived the ideal free distribution where each settled individual has the same fitness, irrespective of habitat quality. This theory can also be applied to foraging predators (Sutherland 1983) and leads us to expect that Oystercatchers aggregate in the sites with the richest food supply, such that intake rate is equalized across sites. These predictions change when individuals differ in 'competitive ability' (Sutherland 1982a, ns & Goss-Custard 1984, Goss-Custard et al. 1996). This paper does not attempt a quantitative test of a particular distribution model. Instead, we analyse our observations on the continually changing distribution of the Oystercatchers during the course of the tidal cycle from the theoretical perspective sketched above. For this we determined how intake rate depended on the food supply and Oystercatcher density and how it changed over the course of the tidal cycle. MTHODS Study site and study population The study was on Texel, the most western island in the Dutch Wadden Sea. The study area was 450 m long and had a maximum width of 300 (Fig. 1). The harbour itself was separated from the mudflats to the north-east by a dike ofgranite stones (Fig. 1). The area as we studied it no longer exists, due to the further enlargement ofthe NIOZ harbour in 1991. Most of the area consisted of hard sand, but the low-lying parts close to the dike and along the gully were more muddy. The lower parts of the dike were made out of stones and this allowed for some settlement of Mussels Mytilus edulis. The entire area was divided into squares of 50 by 50 m. The comers of the grid were marked with poles more than 1 m high, while the sides were marked with small sticks not exceeding 25 cm in length at intervals of 12.5 m. The local topography of the area was determined using projections of slides on a coordinate system adjusted F o mussel bed -20- water level (dm below NAP) Fig. 1. Map of the study area; the inset shows its precise location on the island oftexel. Lines ofequal height are indicated, as well as the location and surface area of the mussel beds. --------

ns et at.: FUNCTIONAL AND NUMRICAL RSPONS 443 for perspective, in combination with measurements in the field. The tidal level of the sites was determined on 22 November 1983 by reading from a scale in the NIOZ harbour the water depth at which the sites were uncovered. Since the area did not fully expose on that day, we used a map from Rijkswaterstaat for the lowest lying parts. Throughout we report waterlevels in cm above or below NAP, which corresponds to mean sea level. The actual water levels during the observation periods were calculated from measurements taken by Rijkswaterstaat at Oudeschild about 5 kin north-east of the study area. The calculations took into account delay and differences in the tidal amplitude between the two locations (see ns et ai. 1996). Polders behind the dikes are used for agriculture, and for breeding by the Oystercatchers. Many of these breeding Oystercatchers were caught on the nest and were subsequently individually marked. We also caught and individually marked many birds outside the breeding season, using mistnets on the feeding grounds and a cannon net on the roost. These birds included nonbreeding immatures, migrants from other parts of urope and birds that probably bred at a considerable distance from our study area so that we failed to locate their nesting territory. Study period The study lasted from February 1983 until July 1984 (ns et al. 1996). However, we only performed systematic counts of the birds in 1983. It was further decided to restrict the analysis of the functional and numerical response to the nonbreeding season, when the birds ate only Cockles Cerastoderma eduie and Mussels and did not defend territories on the mudflats, i.e. from the end of July until the end of October 1983. Sampling the prey ns et ai. (1996) describe in detail when and how the density, size distribution and biomass content ofthe various prey were sampled. A problem for our analysis is that only 11 of the 37 squares that were sampled in April 1983 were 200 Q).c 150 Ci. en.!: 100 40....c g. 35 en.!:... 30..c: 0, c:..92 25 25 30 35 length (mm) in April 0!F'---"--------::-=-=---""""7.'::::---- o 50 100 150 200 density (m-2) in April Fig. 2. (A) Cockle density in September 1983 plotted against the initial density in April 1983 for all squares with densities of at least 10 Cockles m,2. The straight line depicts the prediction from the estimated average mortality of 32.8% (S = 7.2). (B) Mean cockle length (mm) in September 1983 plotted against the mean length (mm) in April 1983. Open dots indicate squares where the length estimate in September is based on less than 20 Cockles. Also depicted is the linear regression line: Y=7.04 + 0.84X, r =0.98, p < 0.001, n =10. sampled in early September 1983. But as cockle densities had declined by 33% between the two sampling periods, irrespective of mean size (Fig. 2A), we used this figure to estimate the September densities from the April densities for the other sites, assuming that the variation in Fig. 2A was primarily due to sampling error. Similarly, cockle size in September for sites not sampled in September could be estimated from the size of Cockles in April (Fig. 2B). Clearly, large Cockles had grown less than small Cockles. 40

444 ARDA 84A, 1996 Observing the birds Distribution of the birds From the moment the first square exposed, the number of Oystercatchers and their activity were noted for all wholly or partly exposed squares every 20 min, until all squares were again covered by the incoming tide. The following activities were recorded: feeding, preening, sleeping, looking and aggression. This procedure was followed on 15 days from late April to the end of October. Nine of these counts took place in the nonbreeding season, including two stormy days where the area hardly exposed. Feeding behaviour of individuals The basic units of analysis are 10 minute periods during which we obtained estimates ofthe capture rate (number of prey captured S l searching), intake rate (in mg AFDM consumed sol feeding) and the density of birds before and after the feeding observation. This information was linked to the water level (via the time), as well as the size and the density ofthe Cockles (via the square). Details on the behavioural protocol, the method to convert prey size estimates into biomass, and data selection, are given by ns et at. (1996). RSULTS Distribution of the prey Mussels Most Mussels occurred above -60 cm NAP in two beds in the centre of the study area and in a few scattered small patches (Fig. 1). In April, densities on the bed ranged from 900 to 2400 individuals m- 2, including all age classes. Cockles Cockles reached high densities in muddy parts close to the dikes, as well as on the low-lying sandy parts of the study area (Fig. 3). Few Cockles were present in squares which had either a high coverage of Mussels or which exposed early and were sandy. The average size of Cockles increased with decreasing shore level of the square (Fig. 4). This has already beenreported (Wanink & Zwarts (1993) and references therein), and is probably due to the better feeding condi- A B c 000 183710 11 811 0> 030 02719 62211 1 2 0 o 1 0 6 1 3 Fig. 3. Number of Cockles in each sample of 0.105 m 2 taken in the study area in late April 1983. D 010 324 238 020 co 014 123 045 634 000 2 1 2 429 510 1 0 1 2 0 5 452 310 I'-- 002 o 0 2 3 1 5 701 010 o 0 1 000 613 3218 5 o 0 2 1 1 0 214 783 co 4616 2 000 013 3 313 607 3630 2 001 6 3 3 001 548 2419 4 o 0 0 014 301 1 1 2 16 8 2 U') 201216 o 0 1 o 710 1 2 6 1 2 1 11 6 8 44 524 o 0 0 001 114 7 1 5 5 13 5 7 19 910 001 004 61911 131934 61510 "<t 2519 3 4 0 0 001 1027 4 918 5 387 920 10 4 2 o 0 9 1 4 8 - - - 3 3 20 6 1 10 0 0 100 ('t) 510 7 o 0 2 o 0-17 413 o 0 0 o 0-080 o 2 0 000 C\I 266 000 000 517 4 o 0 0 052 4 121 o 1 1 000-1018 52321 117 5,... 0 458 7 1358 40 35 '5 c t5 8 30 lij 25 o o o 20 40 60 80 depth below NAP (em) F 100 Fig. 4. Mean size of the Cockles (rom) plotted against the tidal height of the square in cm below NAP. Open dots refer to squares where five or fewer Cockles were sampled, while closed dots refer to squares with more than five Cockles.

ns et at.: FUNCTIONAL AND NUMRICAL RSPONS 445 Table 1. Densities of large Shorecrab (carapace width exceeding 20 mm), Baltic Tellin and Ragworm in the study area in spring 1983. For each species a low, a medium and a high density range were defined and the number of squares counted with a prey density within that range. low density medium density high density samples species range, m- 2 n range, m- 2 n range, m- 2 n Shorecrab a 22 1 11 2 3 36 Baltic Tellin 0-50 11 50-100 8 100-150 5 24 Ragworm 0-50 9 50-100 3 100-150 1 13 tions for Cockles downshore associated with the longer immersion times. In August, it became evident that a considerable spatfall of Cockles had occurred on the higher central parts of the study area (ns et al. 1996). Other prey When Oystercatchers prey on Shorecrabs Carcinus meanas, they only take the very I large and adult individuals (Hulscher 1964). Such crabs were exceedingly rare in the study area (Table I) and occurred only low down the shore., Similarly, Baltic Tellins Macoma balthica nowhere reached densities exceeding 150 individuals m- 2, which Hulscher (1982) considers the density below which these bivalves cannot be profitably exploited by Oystercatchers. Furthermore, whereas the densities in Table 1 refer to all specimens that were retained by the I mm sieve, the threshold value of Hulscher only refers to Macoma with a shell length of at least 10 mm, as this is the minimum size taken by the birds. Finally, the majorityofsites had fewer than 50 Ragworms Nereis diversicolor m- 2, much less than the densities of 100-300 worms m- 2 reported by Bunskoeke et al. (1996) for a study area on Schiermonnikoog, where this worm was one of the staple foods of the Oystercatchers during the breeding season. Diet The low densities of the alternative prey explain why Cockles and Mussels were the most important food items in our study, even in spring (Fig. 8 in ns et al. 1996). Remarkably, large Cockles were completely dropped from the diet during spring (ns et al. 1996). This was also the time of year that alternative prey were most likely to be included in the diet, especially Baltic Tellins. Outside this time of year, the large burying depth and low activity of both Baltic Tellins and Ragworms strongly reduces their availability to Oystercatchers (Zwarts & Wanink 1993, Bunskoeke et al. 1996). The small Cockles of the new spatfall were hardly preyed upon in 1983. The few feeding observations available were mainly obtained on two stonny days when only the top of the shore exposed. Although the small Cockles were then captured at the very high rate of 2.5 Cockles min-i feeding, intake rate was extremely low: 0.6 mg AFDM S l (SD =0.3, n =9). These low intake rates explain why the small Cockles were not preyed upon under more normal circumstances. In the following calculations on the functional and numerical response, we therefore restrict ourselves to the large Cockles. Total bird numbers During May and June the total number of Oystercatchers feeding in the study area fluctuated between 50 and 100 over the low water period. During this nesting season, several marked breeding birds defended territories on the mudflats. From the middle of July onwards, numbers were much higher, fluctuating between 150 and 250. xcept for two stonny days, when only a small part of the study area exposed for a short time and few birds fed there, usage of the area, expressed either as mean bird numbers or number --------------

------_._- 446 ARDA 84A. 1996 ------ ------ 4 MUSSLS 3 2 o 1 : 0u. «14 30 24 30 13 16 8 =n Ol 0.s 6 COCKLS 5 "'" l'li 4 14 10 10 7 15 14 28 7 15 =n O..L---::7---'-7-=-"""""'---,',:--"---!-::----'-----'-''-o-..L- o m M 00 100 1m water level below NAP (em) Fig. 5. t lntake rate (mg AFDM s l) as a function of water level (cm with respect to NAP) for Oystercatchers feeding on (A) Mussels and (B) Cockles. Bars represent 1 S. Sample sizes for each data point are given at the bottomofthe graph. Regression linefor Mussels: Y = 3.08-0.016X. r =-0.16. n = 135. p = 0.07; for Cockles: Y = 1.66 + 0.023X. r = 0.36. n = 120, P < 0.0001. of bird hours per low water period, varied little outside the nesting period. Intake rate and bird distribution in relation to water level When water levels dropped, the intake rate of Oystercatchers feeding on Mussels declined (Fig. SA). Since many Oystercatchers in the study area employed the stabbing technique when feeding on Mussels (ns et al. 1996), this may have been due to the Mussels closing their shells when no longer covered with water. In contrast, the intake rate of Oystercatchers feeding on Cockles in- creased as water levels dropped (Fig. SB). Very probably this was not due to a change in cockle behaviour, but to the fact that the birds changed their feeding site. As Fig. 6 shows, the birds continuously redistributed themselves through the exposure period depending on water level. As the tide receded, they first fed on the Cockles high in the tidal zone, next on the mussel bed and finally on the Cockles low in the tidal zone. When the water started coming in, this sequence was re- I versed. Yet, despite this general pattern, there were always some Oystercatchers feeding on the mussel bed, even when the water reached very low levels. A study of the functional response and interference may help to answer two questions: why are intake rates for birds feeding on Cockles higher in low-lying plots and why did not all the I birds switch to feeding in these plots as soon as they were uncovered? The functional response of birds feeding on Cockles First, the intake rate ofoystercatchers feeding on Cockles might have increased with the density ofthe prey. Instead, a non-significant negative relationship emerged, with a large scatter in the data I (Fig. 7A). Cockle length proved an important. 'confounding' factor, because intake rate increased with length (Fig. 7B). When both variables were entered in a multiple regression equation, the sign of both regression coefficients was positive, but the effect ofcockle density remained non-significant (Table 2). In case sample sizes were insufficient on a per site basis we lumped adjoining sites with similar prey characteristics to give seven large sites (Table 3). Intake rate was. again positively correlated with both prey size and prey density, but in neither case were the results significant. These results are clearly consistent with the previous findings that cockle size increases downshore so that the intake rate of Cockle-feeding Oystercatchers increases as the birds follow the falling tide edge.

---------- ----- ns et at.: FUNCTIONAL AND NUMRICAL RSPONS 447 20 10 A 35 B c 35 D F 9 8 20 10 7 37 f!? Q).r: e ei Cl c:: '0 Q) 2 15... 20 10 6 5 4 20 10 just outside study area 1471010741 BB FLOOD 3 40 20 10 30 20 2 20 10 1471010741 BB FLOOD 1471010741 1471010741 1471010741 BB FLOOD BB FLOOD BB FLOOD water level (dm below NAP) Fig. 6. Number ofoystercatchers feeding in each ofthe study squares relative to the water level, separated for the outgoing and incoming tide. Numbers are averaged for the seven tides between the end ofjuly and the end of October 1983 during which birds were counted, i.e. excluding two tides where the area hardly exposed due to stormy weather. Also indicated the number ofbirds feeding just outside the study area, which happened when the water fell to very low levels.

---------- - 448 ARDA 84A, 1996 6 12 10 in 0 8 u. < Ol 6...:...... ':..... o 20 40.,. e. II... 1 60 80 100 120 140 160 cockle density (m-2)., (I),.. 4 (I) r J. CIl.... os.. 12 10 in 8 o u. < Ol os o +,-...... 2.: 0. 30 32 34 36 38 40 cockle size (mm) Fig. 7. Intake rate (mg AFDM ingested S-I foraging) as a function of (A) the density of Cockles (n m- 2 ), (8) the mean length of the Cockles in the study square. ach dot represents one feeding record. Regression line for cockle density: Y = 2.897 - O.OOIX, r = -0.03, n = 115, P =0.73. Regression line for cockle size: Y= -1.820 + 0.135X, r = 0.26, n = 115, P = 0.006. Interference The above analysis ignored the possibility that intake rates in different sites were depressed to a varying degree due to interference as a result of high bird densities. However, when bird density (log transformed) was added to cockle density and cockle size in a multiple regression analysis, it did not affect intake rate (Table 2). Inclusion of bird density did not change the sign of the effect Table 2. Intake rate (mg AFDM S-I) as a function of cockle density (m- 2 ), cockle size (mm) and bird density (log-transformed numbers ha- I mudflat available for feeding). Regression coefficients and significance levels are shown for (A) the equation with only cockle size and cockle density (R2 = 0.074, F2.112 = 4.5, P = 0.01), and (8) all three independent variables (R2 = 0.067, F 3.59 = 1.4,p = 0.25). Presented are the regression coefficients (b), their standard error (S) and the significance level (P). independent variable b S p equation (a) cockle size, mm 0.16 0.05 0.004 cockle density, m- 2 0.00 0.00 0.29 constant, mg AFDM s-i -2.98 1.99 0.14 equation (b) cockle size, mm 0.08 0.06 0.19 cockle density (m- 2 ) 0.001 0.00 0.Q7 bird density (log ha- I ) 0.23 0.45 0.61 constant (mgafdm S-I) -0.77 2.26 0.73 5 o 4 ::i: o u. 3 os 2.= C3:Mussel.-" D4:cockle ",/ B1:Cockle /<" B3:Mussel -.-....-... B4:Mussel ---:;...---- -;:.<" ;t'/ _----... --, C4:Mussel o'-7-----'-l...l...l-w.-:'::-----'--j--'-'-=-j-u-l100::;;'0 10 1000 Oystercatcher density (ha 1) Fig. 8. Intake rate (mg AFDM S I) as a function ofthe density of Oystercatchers (birds ha 1 mudflat available for feeding on a log scale) for sites with at least seven feeding records. For each site the regression lines are depicted over the range ofobserved bird densities. Four slopes were negative, none significant. Three slopes were positive. with one significant. of cockle size on intake rate, but the effect of this variable became non-significant. This may be related to the reduction in sample size, due to the fact that bird density was not always known.

ns et at.: FUNCTIONAL AND NUMRICAL RSPONS 449 Table 3. Intake rate (mg AFDM S l) averaged for combinations of adjoining sites with similar prey characteristics: cockle density (m- 2 ), cockle size (mm), cockle weight (mg AFDM), intake rate, (mg AFDM S-l), feeding records (n). sites m-2 rnm mg mgs- 1 n B2,B3,C2,C3 4.2 33.5 411 1.9 12 B4,B5,B6,B7,B8,C4,C5,C6 10.3 36.2 525 2.1 7 D5,D6,5,6,7 23.0 38.7 631 4.2 11 Al,A2,A3 49.4 31.2 332 3.1 10 D4,4,F4,F5 63.8 39.0 641 3.5 19 Bl,Cl 79.0 30.8 322 2.6 28 A4,A5,A6 107.0 32.1 361 4.5 3 60em NAP SOem NAP 80 CockIes.m-2 0-10 70 10-50 50-150 Ta ;S 60 'w c: 50 150 1 (I) 150 '0 40 'iii "(l).s::: 50 ti 30 10 e :: 0 20 Ul >. 0 10 0 30 32 34 36 38 30 32 34 36 38 40 Cockle size (mm) Fig. 9. Density of feeding Oystercatchers as a function of the mean size of the Cockles (mm) in the study square, for all counts where the water level had dropped to approximately (A) 60 cm below NAP, or (B) 90 cm below NAP. ach dot is one square and different symbols refer to different densities of Cockles. The lines represent the bird density as predicted from the equations in Table 4, for three different cockle densities. C,) Instead ofattempting to hold prey characteristics constant via multiple regression, interference may be investigated on a site by site basis. The advantage ofthis approach is that no statistical assumptions are needed on the shape of the functional response, and no artifacts are introduced due to the variation in range of bird densities between sites. However, the disadvantage is that sample sizes per site were often small. For only three cockle sites did we have seven or more observations and in no case did we find a significant relationship (Fig. 8). Applying the same selection criterion to the mussel sites, four sites could be added to the sample, yielding three more non-significant relationships, as well as one significant, but positive, relationship (Fig. 8). Clearly, there is no evidence for interference in the present data.

450 ARDA 84A. 1996 Table 4. Density of feeding Oystercatchers (F, n ha 1) as a function of the mean density of Cockles (D, n m 2) and the mean size (S, mm). For two different water levels the results of the following multiple regression analysis are presented: F = b o +bp + b 2S. Levels of significance are presented for the two regression coefficients bj and b 2, as well as the total number of squares on which the regression was performed. water level -60cm -90cm b o -27.8-112.1 0.188 0.120 The numerical response of birds feeding on Cockles The distribution over 15 squares with Cockles could be investigated after water levels had dropped to -60 cm NAP. Though Oystercatcher density was positively correlated with both cockle density and cockle size, neither effect was significant (Table 4, Fig. 9A). When water levels had dropped to -90 cm NAP the distribution over 28 squares could be investigated. Oystercatcher density was again positively correlated with both cockle density and cockle size, but only the effect of size was significant (Table 4. Fig. 9B). DISCUSSION Feeding conditions are better downshore In our study area, the distribution of feeding Oystercatchers continually changed over the low water period as the birds followed the tide edge. This has been reported in many other studies (e.g. Goss-Custard 1977, Sutherland 1982b, Meire 1996). There is general consensus that this is due to the fact that the best feeding areas are located downshore, both for Oystercatchers feeding on Mussels (Goss-Custard & Durell 1987, Goss-Custard et at. 1993, Meire 1996) and for Oystercatchers feeding on Cockles (Sutherland 1982b, Meire 1996, Zwarts et at. 1996b). It is easy to see why this should be so. Both bivalves are suspension p p n 0.25 1.39 0.71 15 0.07 3.52 < 0.001 28 Interference Why did we fail to demonstrate interference? Studies of Oystercatchers feeding on Mussels nearly always yield evidence of interference, whether marked or unmarked birds are studied, but this is not true for Oystercatchers feeding on Cockles (ns & Cayford 1996). Whereas low Oystercatcher densities may explain why Sutherland & Koene (1982) failed to detect interference in Oystercatchers feeding on Cockles, this cannot explain our results, since Oystercatcher densities were quite high. Furthermore, we also studied Oystercatchers feeding on Mussels. Our failure to demonstrate interference could have had two causes: (A) there was no interference, (B) there was interference, but we failed to detect it. We are inclined to the latter of these two explanations for the following reasons. We observed Oystercatchers in late summer, early autumn, whereas the studies of Goss-Custard & Durell (1987) show that interference in both adult and juvenile Oystercatchers is most intense in late winter, when the birds are most pressed for energy. Similarly, Dolman (1995) has shown that in Snow Buntings Ptectrophenax nivalis interference is least intense when feeding conditions are good. i.e. again when the birds are least pressed for energy. This could also be the case in Oystercatchers; the birds certainly achieved high intake rates, especially when feeding on large Cockles, compared to other studies (Zwarts et at. 1996a). Finally, wherever possible, we recorded the behaviour of marked birds, but this may have biased our observations towards those most dominant infeeders, so that the time they can feed increases downshore. As a consequence, these bivalves generally grow better and have a higher condition the further they are down the shore (Wanink & Zwarts 1993 and references therein). Since the observation in this study that intake rate increases more with prey size than with prey density is quite general (Zwarts et at. 1996a), it is clear that feeding conditions for the Oystercatchers are better downshore, even when prey densities are lower there (e.g Sutherland 1982b).

ns et al.: FUNCTIONAL AND NUMRICAL RSPONS 451 dividuals that are least susceptible to interference. Many of the marked birds defended feeding territories during the breeding season and remained quite dominant outside the breeding season. It is known that dominant birds suffer least from interference (ns & Goss-Custard 1984, Goss-Custard & Durell 1988). Ideal free distribution If we conclude from our observations that interference was absent or minimal in our study, then according to the ideal free distribution all birds should have moved to feed in downshore sites with large Cockles as soon as these exposed. Although many birds behaved according to this prediction, a substantial minority continued to feed on the mussel bed over low tide. Because dominance is site dependent (ns & Cayford 1996), one explanation is that loss of dominance prevented the locally dominant birds from feeding elsewhere. However, the cost of being less dominant is an increased susceptibility to interference and if there is no or little interference, this cost cannot be high. A more likely explanation is that differences in foraging efficiency linked to differences in feeding specialization were involved. Although the majority of individuals was seen to take both Cockles and Mussels, especially when the number of prey observations was high, it was also clear that many individuals had a clear bias towards one or other of these prey (ns et al. 1996). Furthermore, high numbers of prey observation were only possible when the individual was observed over a long time span. In the short term, individuals were much more likely to specialize on only one of the two prey, as has been shown in many other studies (Sutherland et al. 1996). These feeding specializations quite subtly influence the foraging efficiency of the individual (Wanink & Zwarts 1996). Thus, individuals that remained to feed on the mussel bed were probably more efficient at locating and handling Mussels than individuals that preferentially fed on Cockles, and vice versa. ACKNOWLDGMNTS Piet Zegers helped catching and marking the birds. Julia Geerding and Jeona Bottema assisted in observing the birds. Aad Sleutel taught us how to build our own hide. Many thanks to Michel Binsbergen, Koos Zegers, Aad Sleutel and others ofthe fonner Research Institute for Nature Management for much practical assistance in the field. Leo Zwarts and John Goss-Custard commented on the manuscript. RFRNCS Bunskoeke.J., BJ. ns, J.B. Hulscher & S.J. de Vias 1996. Why do Oystercatchers Haematopus ostralegus switch from feeding on Baltic Tellin Macoma balthica to feeding on the Ragwonn Nereis diversicolor during the breeding season? Ardea 84A: 91-104. Dolman P.M. 1995. The intensity of interference varies with resource density: evidence from a field study with Snow Buntings, Plectrophenax nivalis. Oecologia (Berl.) 102: 511-514. ns RJ. & J.T. Cayford 1996. Feeding with other Oystercatchers. In: J.D. Goss-Custard (ed.) The Oystercatcher: from individuals to populations: 77 104. Oxford University Press, Oxford. ns BJ. & J.D. Goss-Custard 1984. Interference among Oystercatchers, Haematopus ostralegus, feeding on Mussels, Mytilus edulis, on the xe estuary. J. Anim. col. 53: 217-231. ns RJ., S. Dirksen, C.J. Smit &.J. Bunskoeke 1996. Seasonal changes in size selection and intake rate of Oystercatchers Haematopus ostralegus feeding on the bivalves Mytilus edulis and Cerastoderma edule. Ardea 84A: 159-176. Fretwell S.D. 1972. Populations in a seasonal environment. Princeton University Press, Princeton, New Jersey. Fretwell S.D. & H.L. Lucas 1970. On territorial behavior and other factors influencing habitat distribution in birds. 1. Theoretical development. Acta Biotheoretica 19: 16-36. Goss-Custard J.D. 1977. The ecology of the Wash. III. Density-related behaviour and the possible effects of a loss offeeding grounds on wading birds (Charadrii). J. appl. col. 14: 721-739. Goss-Custard J.D. 1980. Competition for food and interference among waders. Ardea 68: 31-52. Goss-Custard J.D. & S..A. Ie V. dit Durell 1987. Agerelated effects in Oystercatchers Haematopus ostralegus, feeding on Mussels, Mytilus edulis. 1. Foraging efficiency and interference. J. Anim.

- --- - - - ------ 452 ARDA 84A, 1996 co1. 56: 521-536. Goss-Custard J.D. & S..A.le V. dit Durell 1988. The effect of dominance and feeding method on intake rates of Oystercatchers, Haematopus ostralegus, feeding on Mussels. J. Anim. co1. 57: 827-844. Goss-Custard J.D., A.D. West & S..A Ie V. dit Durell 1993. The availability and quality of the mussel prey (Mytilus edulis) of Oystercatchers (Haematopus ostralegus). Neth. J. Sea Res. 31: 419-439. Goss-Custard J.D., AD. West & w.j. Sutherland 1996. Where to feed. In: ld. Goss-Custard (ed.) The Oystercatcher: from individuals to populations: 105-132. Oxford University Press, Oxford. Hulscher J.B. 1964. Hoe een Scholekster Strandkrabben ving. De Levende Natuur 67: 49-52. Hulscher J.B. 1982. The Oystercatcher Haematopus ostralegus as a predator of the bivalve Macoma balthica in the Dutch Wadden Sea. Ardea 70: 89 152. Meire P.M. 1996. Distribution of Oystercatchers Haematopus ostralegus over a tidal flat in relation to their main prey species, Cockles Cerastoderma edule and Mussels Mytilus edulis: did it change after a substantialhabitatloss? Ardea 84A: 525-538. Stephens D.W. & J.R. Krebs 1986. Foraging theory. Princeton University Press, Princeton, New Jersey. Sutherland W.J. 1982a. Spatial variation in the predation of Cockles by Oystercatchers at Traeth Melynog, Anglesy. I. The cockle population. J. Anim. Beo1. 51: 481-489. Sutherland w.j. 1982b. Spatial variation in the predation of Cockles by Oystercatchers at Traeth Melynog, Anglesy. II. The pattern of mortality. J. Anim. Beo1. 51: 491-500. Sutherland WJ. 1983. Aggregation and the ideal free distribution. J. Anim. Beo1. 52: 821-828. Sutherland WJ. & P. Koene 1982. Field estimates of the strength of interference between Oystercatcher Haematopus ostralegus. Oecologia 55: 108-109. Sutherland WJ., BJ. ns, J.D. Goss-Custard & lb. Hulscher 1996. Specialization. In: J.D. Goss-Custard (ed.) The Oystercatcher: from individuals to populations: 56-76. Oxford University Press, Oxford. Wanink J.H. & L. Zwarts 1993. nvironmental effects on the growth rate of intertidal invertebrates and some implications for foraging waders. Neth. J. Sea Res. 31: 407-418. Wanink J.R. & L. Zwarts 1996. Can food specialization by individual Oystercatchers Haematopus ostralegus be explained by differences in prey specific handling efficiencies? Ardea 84A: 177-198. Zwarts L. & J.H. Wanink 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. Neth. J. Sea Res. 31: 441-476. Zwarts L., BJ. ns, J.D. Goss-Custard, J.B. Hulscher & S..A Ie V. dit Durell 1996a. Causes of variation in prey profitability and its consequences for the intake rate of the Oystercatcher Haematopus ostralegus. Ardea 84A: 229-268. Zwarts L., J.B. Hulscher, K. Koopman & P.M. Zegers 1996b. Short-term variation in the body weight of Oystercatchers Haematopus ostralegus: effect of exposure time by day and night, temperature and wind force. Ardea 84A: 357-372. SAMNVATTING Dit onderzoek beoogde de verspreiding van de Scholeksters over het 'NIOZ-wadje' te begrijpen (Fig. 1). Hoewel ook Nonnetjes, Zeeduizendpoten en Strandkrabben voorkwamen, bestond het hoofdvoedsel van de Scholeksters in de herfst en winter vrijwel uitsluitend uit Kokkels en Mossels, waarschijnlijk omdat de dichtheid en actviteit van de alternatieve prooien laag was (Tabel 1). Hoge Scholeksterdichtheden werden bereikt op een klein mosselbankje in het centrum van het gebied, vooral aan het begin en eind van het getij (Fig. 6). Ais de waterstand nog hoog was, hadden de Scholeksters ook de hoogste opnamesnelheid op het mosselbankje (Fig. 5A). Scholekster die op Kokkels foerageerden haalden de hoogste opnamesnelheid als de Kokkels groot waren (Fig. 7B). Merkwaardig genoeg was er geen verband met de Kokkeldichtheid (Fig. 7A, Tabel 2). Ook werden er geen aanwijzingen gevonden voor interferentie, d.w.z. een afname in de opnamesnelheid van voedsel als gevolg van een toename van de dichtheid Scholeksters (Fig. 8). Omdat de Kokkels groter waren naarmate ze lager in de getijzone voorkwamen (Fig. 4), hadden de op Kokkels foeragerende Scholeksters ook een hogere opnamesnelheid naarmate het water lager stond (Fig. 5B). Omdat de opnamesnelheden het hoogst waren als de Scholeksters op die grote Kokkels foerageerden en omdat aanwijzingen voor interferentie ontbraken zouden volgens de meest simpele voorspelling van de 'ideale vrije verdeling' alle Scholeksters in de vakken met grote Kokkels moeten foerageren zodra dat kon. Hoewel een groot aantal Scholeksters dat inderdaad ook deed, bleef er toch ook een aanzienlijk aantal Scholeksters op de mosselbank: en in minder goede kokkelgebieden foerageren (Fig. 9, Tabel 4). Oitheefi waarschijnlijk te maken met verschillen in voedselspecialisatie en, mogelijk, lokale dominantie. I I