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The distribution of the amphipod Corophium arenarium in the Dutch Wadden Sea: relationships with sediment composition and the presence of cockles and lugworms
281
Netherlands Journal of Sea Research 31 (3): 281-290 (1993)
THE DISTRIBUTION OF THE AMPHIPOD COROPHIUM ARENARIUM IN THE DUTCH WADDEN SEA: RELATIONSHIPS WITH SEDIMENT COMPOSITION AND THE PRESENCE OF COCKLES AND LUGWORMS E.C. FLACH Netherlands Institute for Sea Research, P.O. Box 59, 1790AB Den Burg, Texel, The Netherlands ABSTRACT On the tidal flats in the Dutch Wadden Sea Corophium volutator is a dominant species of the upper intertidal zone; the closely related Cor_ophium arenarium is usually found in the lower zone, but only in low densities (a few hundreds per m 2). A survey in the Dutch Wadden Sea showed that this zonation pattern was only present when a muddy sediment was found in the upper zone and a sandy in the lower zone. C. arenarium was restricted to sandy sediments, C. volutatorto muddy sediments. Where a sandy sediment was found in the upper intertidal zone, C. arenarium locally occurred in relatively high densities (a few thousands per mL). An aquarium experiment showed that C. arenarium actively avoided muddy sediments. Field experiments were carried out to study the influence of other macrozoobenthic species (known to affect the related C. volutator) on the abundance of C. arenarium. Within large defaunated areas small plots were stocked with different densities of the lugworm Arenicola marina and the cockle Cerastoderma edule. In small plots within a natural benthic community densities of these species were also augmented or (in A. marina) reduced. Strongly negative density-dependent effects of both A. marina and C. edule were found on the abundance of C. arenarium. In the natural situation, its densities showed A. marinato be the most important factor in determining the abundance of C. arenarium. In particular the removal of lugworms caused a strong increase in C. arenarium densities. These results agreed with the distribution of these species along a transect perpendicular to the shore of Schiermonnikoog, where a significant negative correlation was found between the densities of A. marina and C. arenarium. Aquarium experiments showed that the negative effect of cockles and lugworms must be due to migration rather than mortality in C. arenarium. 1. INTRODUCTION
color O.F. MLiller on the abundance of C. volutator and JENSEN & KRISTENSEN(1990) show that the presThe amphipod Corophium arenarium Crawford lives ence of the tellinid bivalve Macoma balthica L. in burrows in soft sediments along the European reduces the recruitment of C. volutator. In the Wadcoast from the southern part of Jutland to Brittany den Sea, however, N. diversicolor occurs in the high(STOCK, 1952) and along the British Isles (WATKIN, est densities in the muddy upper-tidal zone, where 1941 ; FISH& MILLS, 1979). It often occurs together with also the highest numbers of C. volutatorcan be found the closely related C. volutator Pallas, although within (THAMDRUP, 1935). M. balthica, on the other hand, is one locality they mostly show spatial segregation. C. rather evenly distributed on the tidal flats in the Dutch arenarium inhabits the sandy sediments and C. volu- Wadden Sea at densities of -150 per m 2 (DANKERS& tator seems to be confined to the more muddy sedi- BEUKEMA,1983). It therefore seems unlikely that these ments (WATKIN, 1941). JENSEN & KRISTENSEN (1990), two species restrict C. volutator to the upper zone. however, conclude that the spatial segregation of the Two other species that have strong negative impacts two Corophium species cannot be explained by differ- on the abundance of C. volutator, the cockle Cerastoences in abiotic factors in the Danish Wadden Sea. derma edule L. (JENSEN, 1985; FLACH, 1992) and the Although C. volutator is competitively superior to C. lugworm Arenicola marina L. (FLACH, 1992), are domiarenarium, C. arenarium maintains its position on the nant in the lower, sandier part of the tidal flats in the tidal flats. They therefore suggest that another factor Wadden Sea (THAMDRUP, 1935; LINKE, 1939; REISE, is involved, e.g. the predation by the dunlin Calidris 1978). In this lower, sandier zone C. arenarium can alpina (L.). Also other infaunal species may influence normally also be found. Because of the differential zonation patterns found C. volutator negatively, restricting its distribution. OLAFSSON & PERSSON (1986) and RONN et aL (1988) in the Wadden Sea and the reported competitive report a negative effect of the ragworm Nereis diversi- superiority of C. volutatorover C. arenarium, I studied
282
E.C. FLACH
North Sea
Ameland
-Iolwerd
o,~' ~ ~. [--:~
Oever
JNer,ooOs
Fig. 1. The location of the two experimental spots A and B and the geographical names of the places where the transects (lines perpendicularto the shore) were sampled in the Dutch Wadden Sea. The Mean-Low-Water line is indicated by broken lines. the effects of C. edule and A. marina also on the other species of Corophium, C. arenarium. This study took place on tidal flats in the Dutch Wadden Sea. 2. MATERIALS AND METHODS 2.1.SURVEYS At Balgzand a transect of 800 m perpendicular to the shore was sampled every month from 1989 onwards to study the dynamics of the Corophium populations in relationship with the densities of cockles and lugworms. The distance between the samples was N20 m. In July 1991 and 1992, surveys were carried out in the Dutch Wadden Sea to study the distribution of the two Corophium species. Samples were taken along transects of ~1 km perpendicular to the shore. Distances between the samples were N50 m and no. 1 was always close to the shore. Three samples of 85 cm 2 to a depth of -10 cm were taken and sieved through a 500-~m mesh sieve in the field. At the same places the number of lugworm castings per m2 and the numbers of cockles in 0.25-m 2 plots were counted. The samples were preserved in 4% formaldehyde and counted with a binocular microscope (10x) in the laboratory. All Corophium individuals
were measured from tip of rostrum to end of telson. Animals larger than 4 mm were sexed and females with eggs in their broodpouch were counted separately. The eggs were counted and divided into four developmental stages after FISH & MILLS (1979). Only animals larger than - 3 mm could be identified to species. The species were distinguished by the difference in the structure of the peduncle of the first uropode: C. arenarium has a number of setae proximally at the edge of the peduncle which are lacking in C. volutator (STOCK, 1952). 2.2. FIELD EXPERIMENTS Field experiments were carried out on tidal flats at Balgzand (A) in the westernmost part of the Wadden Sea in 1990 and near the island of Schiermonnikoog (B) in 1992 (Fig. 1). At these sites a PVC-mat was placed over the sediment during winter. After removal of the mats in March, homogeneous, depopulated (azoic) squares of -100 m2 were obtained. Within these squares, small plots of 1 m 2 each were restocked with four different densities of A. marina (25, 50, 75 and 100 per m2) and C. edule (250, 500, 750 and 1000 cockles of 2 cm length per m2). In the square at Balgzand also three different densities of A.
COROPHIUMARENARIUM IN THE DUTCH WADDEN SEA
marina plus C. edule (12 lugworms + 125 cockles, 25 + 250 and 50 + 500 per m 2) were stocked in the small plots. The animals were collected at nearby tidal flats and transported to the plots as fast as possible. The restocking was done two weeks after removal of the mat in which time an oxygenated top layer had developed in the sediment. All densities were applied in duplicate and there were empty spaces of 50 cm width between the small plots to avoid interactions. Three of these small plots remained empty to serve as controls. On the tidal flat near the island of Schiermonnikoog
283
the densities of cockles and lugworms were also manipulated in the otherwise undisturbed natural situation. The naturally occurring densities of these species were estimated first, after which these densities were augmented in small plots of 1.5 x 1.5 m to reach densities of A. marina of 50, 75 and100 per m 2 and of C. edule of 500, 750 and 1000 per m 2. All densities were applied in duplicate, the natural situation around these plots was used as a control. In three small plots the numbers of A. marina were diminished by stabbing the lugworms to death with thin pins, which resulted in densities of ~10 per m 2 (natural densities
TABLE 1 The sediment composition along various transects of ~1 km from the shore to the tidal channel in different parts in the Dutch Wadden Sea and the Corophium species and densitiy found at that place. (No. 1 is close to the shore, no. 10 (Balgzand 20) is the middle of the transect and no. 20 (Balgzand 40) is the end of the transect. Not all transects were this long: Noordsvaarcler, Koffieboonplaat and Den Oever were only 300 m). Place
Den Oever Balgzand
No
% silt (<50 IJ.m)
1
med. grain size (m)
muddy
Corophium sp. C. volutator
n per m2
45412
1 20 40
11.2 3.5 1.1
141.7 157.3 175.9
C. volutator no Corophium C. arenarium
510
Texel
1 10 20
24.8 1.8 1.1
90.6 176.9 178.0
C. volutator C. arenarium C. arenarium
78 550 745
Vlieland
1 10 20
12.3 5.2 2.2
184.4 182.6 137.9
algae cover C. arenarium no Corophium
78
1 10 20 1 1
18.4 4.6 1.3 1.2 1.1
161.7 189.4 184.8 209.6 216.7
C. volutator C. arenarium C. arenarium C. arenarium C. arenarium
Ameland
1 10 20
4.2 2.5 4.4
184.1 176.1 177.2
C. arenarium C. arenarium no Corophium
157 39
Holwerd
1 10
28.8 4.0
75.4 110.4
C. volutator C. arenarium
39 78
Schiermonnikoog
1 10 20
2.9 2.5 1.3
169.8 169.9 170.0
C. arenarium C. arenarium no Corophium
1843 274
Hornhuizen
1 10
C. arenarium C. arenarium
78 235
Noordpolderzijl
1 10 20
Terschelling
Noordsvaarder Koffieboonplaat
rather sandy rather sandy 75.1 19.2 4.1
33.3 90.3 114.4
C. volutator C. volutator no Corophium
120
2862 510 157 470 1137
62471 28941
284
E.C. FLACH
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Fig. 2. Distribution pattern of A. marina and C. edule (a) and the two Corophium species (b) along a transect from the shore (near high-tide level, no. 1 ) to the tidal channel (near low-tide level, no. 40) at Balgzand, May 1990. Distance between the samples is - 2 0 m.
ence of the two Corophium species. The first experiment was carried out in three aquaria (A, B and C) of 40 x 20 x 30 cm (I x w x h), filled with a layer of 15 cm sieved sandy sediment. Partitions of 20 cm height were placed in the sediment halfway the length of the aquaria. The aquaria were filled with filtered sea water to the upper edge of the partitions (-5 cm). At the right-hand side of aquarium C, 15 C. edule of -3 cm length (-12% coverage) were placed, at that of aquarium B 4 A. marina (-100 per m2), whereas the right-hand side of aquarium A remained empty. The left-hand side was kept empty in all aquaria. Twenty C. arenarium (-500 per m 2) were released at the right-hand side of the aquaria, where they were first allowed to settle. After -24 h the water level was raised to ~10 cm above the partition, enabling C. arenarium to swim freely to the left-hand side. The aquaria were placed in a row with the light from above and they were aerated in the middle of the aquarium. After two weeks the numbers of C. arenarium at the two sides of the partition were counted. This experiment was repeated 14 times. The Wilcoxon-MannWhitney test (SIEGEL& CASTELLAN, 1988) was used to test whether the numbers of migrated Corophium were different in the aquaria with cockles or lugworms as compared to the 'empty' control aquarium. The second type of experiment was performed in two aquaria of 40 x 10 x 30 cm in which two partitions of 10 cm height were placed to obtain three equally sized compartments. These compartments were filled with three different types of sieved sediment: a silty sediment (from a place where high densities of C. volutatorwere found), a sandy sediment and a mixed sediment composed of the two other types. The arrangement of the sediment types differed in the two aquaria. The aquaria were placed next to each other with the light from above and they were aerated in the middle of the aquarium. The aquaria were filled up with a layer of 15 cm filtered sea water, and 20 C. arenarium or C. volutatorwere released in the water column, so that they could settle freely in any of the three sediment types. After two weeks the numbers of Corophium in each of the three compartments were counted. This experiment was repeated 15 times and
-30 per m2). All plots were sampled once in early July and once at the end of August. From each plot three samples were taken of 255 cm 2 each to a depth of -10 cm. These samples were treated as described above for the surveys. At the time of sampling the number of lugworm castings in the plots was counted as well, and also the numbers of cockles in the samples. The 35C0 length of the cockles was measured to calculate the 3ooo area fraction covered by the cockles as described by 250O JENSEN(1985). A non-parametric trend-test, which is a modification "E 20oo of the Kruskal & Wallis test, described by DE JONGE c 1500(1963: p. 340), was used to evaluate the effects of the IOOO" densities of cockles and lugworms. A short descrip5OOtion of this rank test is given by BEUKEMA(1968: p. 9). o
2.3. LABORATORY EXPERIMENTS Two kinds of laboratory experiments were carried out, one to study effects of cockles and lugworms on C. arenarium and the other to study the sediment prefer-
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Fig. 3. Distribution pattern of the two Corophium species
along a transect from the shore (no. 1) to the tidal channel (no. 20) near the island of Terschelling, July 1992. Distance
between the samples is - 50 m.
COROPHIUM ARENARIUM IN THE DUTCH WADDEN SEA
the sign test (SIEGEL& CASTELLAN, 1988) was used to test whether the numbers of settled Corophium were different between different sediments offered.
285
C. a c e n a d u m n per m*
60
50'
3. RESULTS
40
3.1. SURVEYS
30 20
Fig. 1 shows the spots where Corophium was sampled during the survey of July 1992 in the Dutch Wadden Sea. At most tidal-flat stations C. arenarium was found in low densities; C. volutator was found only in a few places, though then mostly in high densities. If C. volutatorwas found, it was invariably at the highest places close to the shore in muddy sediments, whereas C. arenarium was found in sandy sediments only (Table 1). These sandier parts are mostly also the lower parts of the tidal flats at which also rather high densities of A. marina and C. edule can be found. Fig. 2 gives an example of the distribution of the two Corophium species, and of lugworms and cockles along a transect at Balgzand from the shore (high-tide level, no. 1) to the tidal-channel (low-tide level). Elsewhere the two species occurred in the same zone (Fig. 3). At two places relatively high densities of C. arenarium were found, viz. on the Koffieboonenplaat at the eastern part of Terschelling and at a tidal flat near Schiermonnikoog. In these areas, the highest densities were found at high levels close to the shore (Fig. 4), which had unusually sandy sediments for such high intertidal levels (Table 1). Fig. 4 also shows that the densities of C. arenarium along their transect were negatively related to the densities of A. marina (Spearman rank-correlation coefficient r= -0.73, p
50
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% • 10CO ~.
=
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Fig. 4. Distribution patterns of A. marina and C, arenarium along a transect from the shore (no. 1) to the tidal channel (no. 20) near the island of Schiermonnikoog, July 1991. Distance between the samples is -50 m.
10 0
, 200
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Fig. 5. Relationships observed in square A between the densities (n.m-2) of C. arenarium and actual densities at the time of sampling (July 1990) of (a) C. edule (R = -0.62, p
286
E.C. FLACH
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August is given in Fig. 7b. In the otherwise undisturbed natural plots, in which only the densities of cockles and lugworms were manipulated, only the effect of the removal of lugworms was significant (13<0.01) in July (Fig. 6b). In the three small plots from which only the lugworms had been removed, the densities of C. arenarium were about 10x higher than in the natural situation. These high densities were similar to those found in the empty plots of the defaunated square. Fig. 8 shows the relationship between the actual densities of A. marina and the C. arenarium densities in all natural plots in August. Although the lugworm densities were different in the cockle plots, the densities of C. arenarium were about equally low in all cockle plots (area fraction covered by C. edule between 12 18%). Although there were strong differences in total numbers, the population structures of C. arenarium
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Fig. 6. The mean densities (n.m-2 with one standard error) of C C. arenarium (a) in the small plots within the defaunated E 6OO, square populated with different initial densities of A. marina _= and C. edule (number of replicates n=2) compared to the f~ 4OO empty (azoic) plots (n=3) and (b) in otherwise undisturbed 9o 20O plots with additions of Arenicola (At.+) and Cerastoderma u (Cer.+) (n=6) and removal of Arenicola (Ar.-) (n--3) of these species compared to the fully natural situation (nat.) (n=6). 0 All observations made at site B near the island of Schiermonnikoog, July 1992.
!
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I
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20
30
40
50
Arenlcola
n per m s
the natural situation around the square. A strongly 1200 b negative effect of the presence of A. marina was found. Their initial approximately natural density of 25 ~ looo had diminished to N18 lugworms per m 2 and even this low density caused a reduction of N50% in C. are- ~ 800 narium densities. The initial enhanced densities of 50, C 75 and 100 lugworms had diminished to 40, 46 and E 600 43, respectively, in July, causing the numbers of C. arenarium to be about equal in these plots (Fig. 6a). } 4oo In these lugworm plots the densities of C. arenarium 0 were about the same as in the natural situation (-30 u 20O lugworms per m2). With the actual lugworm densities, | 13 a significant density-dependent negative effect on the 0 5 10 15 densities of C. arenarium was found (p<0.01, trend% occ. by Cerast. test). A negative relationship between the actual lugworm densities present in the small plots and the densities of C. arenarium was also found in August Fig. 7. The densities (n-m-2) of C. arenarium in the small (Fig. 7a). Also a significant (p<0.05, trend-test) nega- plots within the defaunated square stocked with different initive density-dependent effect was found of C. edule tial densities of A. marina (a) and C. edule (b). Given are the on the numbers of C. arenarium, although the lowest actual densities of A. marina and the actual % of area covdensity (250 cockles with ~1.1% area coverage) did ered by C.edule at site B in August. The % area coverage of not differ from the empty plots (Fig. 6a). The relation- C. edule was calculated after JENSEN (1985) by counting ship between the actual proportion of area coverage and measuring the cockles from each plot. The numbers of by C. edule and the numbers of C. arenarium in A. marina were estimated by counting the castings•
COROPHIUM ARENARIUM IN THE DUTCH WADDEN SEA
nificantly higher numbers of C. volutator settled in the silty sediment as compared to the sandy sediment (p
1000 800
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287
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4. DISCUSSION
400
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[~ D
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n por m 2
Fig. 8. The densities (n.m-2) of C. arenarium related to the densities of A. marina in the small plots with additions of A. marina (At) and C. edule (Cer) and from which A. marina (Ar) was removed in the otherwise undisturbed natural situation compared to the fully undisturbed natural situation (nat) at site B in August 1992. were similar in all plots. Neither was there any significant difference in the number of eggs per female between the different treatments. The number of eggs per female were in most cases rather low (<15 per female), and the mean number of eggs per female was only 4.7 + 2.4 (n = 92). This low number was partly due to the small size of most egg-bearing females (mean length 4.5 + 0.8), but even most of the larger females had few eggs. No correlation between the number of eggs and the developmental stage was found, which suggests that no significant loss of eggs occurred during the period of development.
The results of the field experiments, viz. strongly negative effects of both C. edule and A. marina on the ')undance of C. arenarium, were similar to the suits obtained in previous experiments in C. volutar (FLACH, 1992). In the case of C. volutator, however, e experimental results could quite well explain the ;neral distribution patterns found in the Wadden _ ;a with C. volutatoras the dominating species in the upper tidal zone and C. edule and A. marina dominating the bordering lower intertidal zone. C. arenarium, however, was frequently found in the highest numbers exactly in this lower A. marina + C. edule dominated zone (as exemplified in Fig. 2). This raises a problem, because the abundance of both C. volutator and C. arenarium was found to be affected negatively by the presence of A. marina and C. edule (and in the case of A. marina already at low numbers of this species). JENSEN & KRISTENSEN (1990) explain the differential zonation of the two Corophium species by the competitive superiority of C. volutator over C. arenarium. C. volutator inhabits the upper part of the intertidal zone, probably restricted to it by factors such as the presence of lugworms in the lower zone, leaving the lower zone to C. arenarium. These authors did not find any significant differences in abiotic factors 10
3.3. LABORATORY EXPERIMENTS Fig. 9 summarizes the result of the experiment on the effect of the presence of cockles and lugworms on the distribution of C. arenarium. Significantly (p
9 8
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~ 2
6 5
,-
4 3 2 1 0
o
empty
I Arenlc.
I Cerast.
Fig. 9. The mean number (with standard error) of C. arenarium that had migrated in the aquaria with A. marina or C. edule compared to the aquarium without the latter two species (empty). The experimentwas replicated 14 times.
288
E.C. FLACH
between the two places (with rather sandy sediments) where they found the two Corophium species. In the Dutch Wadden Sea, however, C. volutatorwas found to be restricted to muddy sediments and C. arenarium to sandy sediments (Table 1), with little overlap: such differences were also found by WATKIN (1941) in the Dovey Estuary. The aquarium experiments also suggested that C. arenarium prefers sandy sediments and C. volutator muddy sediments (Fig. 10). The composition of the sediments in which JENSEN& KRISTENSEN(1990) observed the two species was similar to those in which only C. arenarium was found in the Dutch Wadden Sea. Along the two transects (Schiermonnikoog, Koffieboonenplaat) with only sandy sediments (even at the higher parts), only C. arenarium was found. In these two areas, the densities of C. arenarium were particularly high in the higher parts. This agrees with the results of the field experiments as the densities of both A. marina and C. edule were low in these higher parts. Removal of lugworms caused -lOx higher C. arenarium densities both in the natural situation and in the defaunated square, whereas these densities were at the same level as in the natural situation in the plots with high lugworm densities. So, it can be concluded that the low natural density must have been due to the presence of A. marina. This was also suggested by the mirrored pattern of densities of lugworm and C. arenarium along the Schiermonnikoog transect (Fig. 4). The strongly negative effect of cockles on the abundance of C. arenarium could not be compared to a natural situation because only low natural cockle densities (-1-2% area coverage) were found. However, the results of the experiments suggest that high cockle densities would further reduce the numbers of C. arenarium (Fig, 8). Although the densities of C. arenarium were much higher in the upper parts of the transects at Koffieboonenplaat and Schiermonnikoog and in the experimental lugworm-free plots than in any place where lugworms were present, maximal densities of C. arenaria were far below the maximal densities of C. volutator. This difference between the two species can be explained by the much lower reproductive capacity of C. arenarium (FISH& MILLS, 1979; JENSEN& KRISTENSEN, 1990). The mean number of eggs per female (-4.7) at a mean length of the females of -4.5 mm found in this study was even lower than that reported by FISH & MILLS (1979), viz. ~12.8 eggs at a female length of 4.7 mm in July. FISH& MILLS(1979) also report a difference in egg number at stages 1 and 4, indicating a loss from the broodpouch of -26%. Such a loss was not found in the present study. Neither did I find any difference in eggnumber between the different treatments, whereas for C. volutator somewhat lower eggnumbers were found in treatments with high cockle or lugworm densities (FLACH, 1993). The effect of cockles and lugworms on the C. volutator population structure (viz. a lower proportion of gravid females and smaller
50 40 .E ~ 30 • o d 20 10
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5.30%
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198,7 ~J
0 sand
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60 m
50
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~ 40 ~ 30 d
~ 20 1o 0
I
sand
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mixed
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silt
Fig. 10. The mean proportion (with standard error) of (top) C. arenarium and (bottom) C. volutatorthat settled in the different sediments in the sediment-choice aquaria. The sediment composition is given in the bars, upper number is % silt (<50 p.m), lower number is median grain size (in #m). The experiments were replicated 15 times. sizes (FLACH, 1993)) was not found in C. arenarium. However in C. volutator, it were especially the bigger individuals (>5.5 mm) that were affected; in C. arenarium such sizes were not found. The results from the aquarium experiments suggest that the negative influences of lugworms and cockles were not caused by a higher in situ mortality rate but rather by a higher migration rate in C. arenarium. This migration was probably induced by the sediment-disturbing activities of lugworms and cockles. A. marina is known for its high bioturbation rate, especially in summer with a daily average of sediment reworking of -27.7 cm 2 per worm (CADI~E,1976). Already at intermediate lugworm densities (-17 per m 2, the mean for the tidal flats of the Wadden Sea
COROPHIUM ARENARIUM IN THE DUTCH WADDEN SEA
289
(BEUKEMA & DE VLAS, 1979)) this activity can cause a work in the nature reserve Schiermonnikoog. And I would severe disturbance of the upper sediment layer. LINKE also like to thank W.J. Wolff and two anonymous referees (1939) already suggested that this sediment-rework- for their useful comments on an earlier version of the manuing activity of A. marina could have negative effects script. on the tube building C. volutator. BREY (1991) con5. REFERENCES cludes that especially the funnels of A. marina cause a strong reduction in number of C. volutator. It is likely BEUKEMA,JJ., 1968. Predation by the three-spined sticklethat the same would apply to the closely related C. back (Gasterosteus aculeatus L.): The influence of arenarium. JENSEN (1985) reports that the burrowing hunger and experience.--Behaviour 31:1-126. and ploughing habits of C. edule negatively affect C. BEUKEMA,J.J. & J. DE VLAS, 1979. Population parameters of volutator. He found high migration rates at high cockle the lugworm Arenicola marina, living on the tidal flats of the Dutch Wadden Sea.--Neth. J. Sea Res. 13" 331densities, but also low in situ survival, growth and 353. reproduction. In the present study, however, only higher migration rates were found at high cockle den- 8REY, T., 1991. The relative significance of biological and physical disturbance: an example from intertidal and sities; no effects on survival or reproduction of C. aresubtidal sandy bottom communities.--Estuar, coast. narium were found. This negative effect resulted not Shelf Sci. 33: 339-360. merely from the presence of cockles as can be seen CADI~E,G.C., 1976. Sediment reworking by Arenicola marina from the relationship between the area fraction covon tidal flats in the Dutch Wadden Sea.--Neth. J. Sea ered by C. edule and the reduction in Co arenarium Res. 10: 440-460. numbers. A reduction in C. arenarium numbers of DANKERS, N. & J.J. BEUKEMA, 1983. Distributional patterns of macrozoobenthic species in relation to some environ- 5 0 % was already found at an area fraction covered mental factors. In: W.J. WOLFF. Ecology of the Wadden by cockles of only 5%, and a reduction of ~80% at Sea. Balkema, Rotterdam, Vol. 1, part 4:69-103. 10% coverage of cockles. This reduction was even stronger than that found previously for C. volutator DE JONGE,H., 1963. Inleiding tot de Medische Statistiek. Verhandelingen van het Nederlands Instituut voor Praewhen a reduction of N50% was reached only at ~13% ventieve Geneeskunde, XLI. Leiden, Deel 1, 2e druk: coverage of cockles (FLACH, 1992). The gravity of the 1-421. influence of A. marina was similar in the two FISH, J.D. & A. MILLS, 1979. The reproductive biology of Corophium species, a reduction of ~50% at lugworm Corophium volutator and C. arenarium (Crustacea: densities of N18 per m 2. On the sandy tidal flats of the Amphipoda).--J. mar. biol. Ass. U.K. 5g: 355-368. German Wadden, REISE (1985) found a mean density FLACH, E.C., 1992. The influence of four macrozoobenthic species on the abundance of the amphipod Corophium of no less than ~40 lugworms per m 2. Such a high volutator on tidal flats of the Wadden Sea.--Neth. J. density reduced C. arenarium numbers in the present Sea Res. 2g- 379-394. study to - 1 0 % of those in areas without lugworms. --, 1993. Effects of Arenicola marina and Cerastoderma In conclusion, C. arenarium prefers a sandy sediedule on distribution, abundance and population strucment. In the Wadden Sea, such sediment is most freture of Corophium volutator in the Gullmarsfjord (SW quently present at the lower parts of the tidal flats. Sweden).--Sarsia 78 (in press). Here densities of lugworms and sometimes also JENSEN, K.T., 1985. The presence of the bivalve Cerastocockles are high too. Both cockles and lugworms derma edule affects migration, survival and reproduction of the amphipod Corophium volutator.--Mar. Ecol. have a strongly negative impact on densities of C. Prog. Ser. 25: 269-277. arenarium. This negative effect is probably caused by sediment-disturbing activities of cockles and lug- JENSEN, K.T. & L.D. KRISTENSEN, 1990. A field experiment on competition between Corophium volutator (Pallas) and worms which force C. arenarium to migrate. RelaCorophium arenarium Crawford (Crustacea: Amphiptively high densities of C. arenarium were found only eda): effects on survival, reproduction and recruitat specific places in the Dutch Wadden Sea, characment.--J, exp. mar. Biol. Ecol. 137: 1-24. terized by high intertidal levels (causing low densities LINKE, 0., 1939. Die Biota des Jadebusenwattes.--Helgoof lugworms and cockles) and a sandy sediment lander wiss. Meeresunters. 1: 201-348. (excluding competition by the related C. volutator). OLAFSSON, E.B. & L.-E. PERSSON, 1986. The interaction between Nereis diversicolor O.F. MUller and Thus, the generally low densities of C. arenarium Corophium volutator Pallas as a structuring force in a observed in nearly all of the Wadden Sea will be shallow brackish sediment.--& exp. mar. Biol. Ecol. caused by the presence of lugworms and cockles in 103" 103-117. far most of the (prevailing) sandy sediments. REISE, K., 1978. Experiments on epibenthic predation in the Wadden Sea.--HelgolAnder wiss. Meeresunters. 31: Acknowledgements.--I am grateful to J.J. Beukema for the 55-101. support received during this study. I would also like to thank , 1985. Tidal flat ecology. An experimental approach to E. Adriaans, C. Baltus, W. de Bruin and J. Zuidewind for species interactions. Ecological studies 54. Springer their assistance with the field work and the crew of the RV Verlag, Berlin: 1-191. 'Navicula' for the pleasant trips to the tidal fiats. The Society for the Protection of Nature Reserves, the Ministry of Agri- RONN, C., E. BONSDORFF& W.G. NELSON, 1988. Predation as a mechanism of interference within infauna in shallow culture, Nature Management and Fisheries and the Municibrackish water soft bottoms; experiments with an infaupality of Schiermonnikoog were so kind as to allow me to
290
E.C. FLACH
nal predator, Nereis diversicolor O.F. MOIler.~. exp. Mar. Biol. Ecol. 116" 143-157. SIEGEL, S. & N.J. CASTELLANJr., 1988. Nonparametric statistics for the behavioral sciences. 2nd Ed. McGraw-Hill Book Co., Singapore: 1-399. STOCK,J.H., 1952. Some notes on taxonomy, the distribution and the ecology of four species of the amphipod genus Corophium (Crustacea, Malacostraca).--Beaufortia, Amsterdam 21: 1-10.
THAMDRUP,H.M., 1935. Beitr&ge zur Okologie der Wattenfauna auf experimenteller Grundlage.--Meddr Kommn Danm. Fisk.-og Havsunders., Ser. Fisk. 10" 1-125. WATKIN, E.E., 1941. The yearly life cycle of the amphipod Corophium volutator.--J, animal Ecology 10: 77-93. (accepted 10 September 1993)
Netherlands Journal of Sea Research 31 (3): 281-290 (1993)
THE DISTRIBUTION OF THE AMPHIPOD COROPHIUM ARENARIUM IN THE DUTCH WADDEN SEA: RELATIONSHIPS WITH SEDIMENT COMPOSITION AND THE PRESENCE OF COCKLES AND LUGWORMS E.C. FLACH Netherlands Institute for Sea Research, P.O. Box 59, 1790AB Den Burg, Texel, The Netherlands ABSTRACT On the tidal flats in the Dutch Wadden Sea Corophium volutator is a dominant species of the upper intertidal zone; the closely related Cor_ophium arenarium is usually found in the lower zone, but only in low densities (a few hundreds per m 2). A survey in the Dutch Wadden Sea showed that this zonation pattern was only present when a muddy sediment was found in the upper zone and a sandy in the lower zone. C. arenarium was restricted to sandy sediments, C. volutatorto muddy sediments. Where a sandy sediment was found in the upper intertidal zone, C. arenarium locally occurred in relatively high densities (a few thousands per mL). An aquarium experiment showed that C. arenarium actively avoided muddy sediments. Field experiments were carried out to study the influence of other macrozoobenthic species (known to affect the related C. volutator) on the abundance of C. arenarium. Within large defaunated areas small plots were stocked with different densities of the lugworm Arenicola marina and the cockle Cerastoderma edule. In small plots within a natural benthic community densities of these species were also augmented or (in A. marina) reduced. Strongly negative density-dependent effects of both A. marina and C. edule were found on the abundance of C. arenarium. In the natural situation, its densities showed A. marinato be the most important factor in determining the abundance of C. arenarium. In particular the removal of lugworms caused a strong increase in C. arenarium densities. These results agreed with the distribution of these species along a transect perpendicular to the shore of Schiermonnikoog, where a significant negative correlation was found between the densities of A. marina and C. arenarium. Aquarium experiments showed that the negative effect of cockles and lugworms must be due to migration rather than mortality in C. arenarium. 1. INTRODUCTION
color O.F. MLiller on the abundance of C. volutator and JENSEN & KRISTENSEN(1990) show that the presThe amphipod Corophium arenarium Crawford lives ence of the tellinid bivalve Macoma balthica L. in burrows in soft sediments along the European reduces the recruitment of C. volutator. In the Wadcoast from the southern part of Jutland to Brittany den Sea, however, N. diversicolor occurs in the high(STOCK, 1952) and along the British Isles (WATKIN, est densities in the muddy upper-tidal zone, where 1941 ; FISH& MILLS, 1979). It often occurs together with also the highest numbers of C. volutatorcan be found the closely related C. volutator Pallas, although within (THAMDRUP, 1935). M. balthica, on the other hand, is one locality they mostly show spatial segregation. C. rather evenly distributed on the tidal flats in the Dutch arenarium inhabits the sandy sediments and C. volu- Wadden Sea at densities of -150 per m 2 (DANKERS& tator seems to be confined to the more muddy sedi- BEUKEMA,1983). It therefore seems unlikely that these ments (WATKIN, 1941). JENSEN & KRISTENSEN (1990), two species restrict C. volutator to the upper zone. however, conclude that the spatial segregation of the Two other species that have strong negative impacts two Corophium species cannot be explained by differ- on the abundance of C. volutator, the cockle Cerastoences in abiotic factors in the Danish Wadden Sea. derma edule L. (JENSEN, 1985; FLACH, 1992) and the Although C. volutator is competitively superior to C. lugworm Arenicola marina L. (FLACH, 1992), are domiarenarium, C. arenarium maintains its position on the nant in the lower, sandier part of the tidal flats in the tidal flats. They therefore suggest that another factor Wadden Sea (THAMDRUP, 1935; LINKE, 1939; REISE, is involved, e.g. the predation by the dunlin Calidris 1978). In this lower, sandier zone C. arenarium can alpina (L.). Also other infaunal species may influence normally also be found. Because of the differential zonation patterns found C. volutator negatively, restricting its distribution. OLAFSSON & PERSSON (1986) and RONN et aL (1988) in the Wadden Sea and the reported competitive report a negative effect of the ragworm Nereis diversi- superiority of C. volutatorover C. arenarium, I studied
282
E.C. FLACH
North Sea
Ameland
-Iolwerd
o,~' ~ ~. [--:~
Oever
JNer,ooOs
Fig. 1. The location of the two experimental spots A and B and the geographical names of the places where the transects (lines perpendicularto the shore) were sampled in the Dutch Wadden Sea. The Mean-Low-Water line is indicated by broken lines. the effects of C. edule and A. marina also on the other species of Corophium, C. arenarium. This study took place on tidal flats in the Dutch Wadden Sea. 2. MATERIALS AND METHODS 2.1.SURVEYS At Balgzand a transect of 800 m perpendicular to the shore was sampled every month from 1989 onwards to study the dynamics of the Corophium populations in relationship with the densities of cockles and lugworms. The distance between the samples was N20 m. In July 1991 and 1992, surveys were carried out in the Dutch Wadden Sea to study the distribution of the two Corophium species. Samples were taken along transects of ~1 km perpendicular to the shore. Distances between the samples were N50 m and no. 1 was always close to the shore. Three samples of 85 cm 2 to a depth of -10 cm were taken and sieved through a 500-~m mesh sieve in the field. At the same places the number of lugworm castings per m2 and the numbers of cockles in 0.25-m 2 plots were counted. The samples were preserved in 4% formaldehyde and counted with a binocular microscope (10x) in the laboratory. All Corophium individuals
were measured from tip of rostrum to end of telson. Animals larger than 4 mm were sexed and females with eggs in their broodpouch were counted separately. The eggs were counted and divided into four developmental stages after FISH & MILLS (1979). Only animals larger than - 3 mm could be identified to species. The species were distinguished by the difference in the structure of the peduncle of the first uropode: C. arenarium has a number of setae proximally at the edge of the peduncle which are lacking in C. volutator (STOCK, 1952). 2.2. FIELD EXPERIMENTS Field experiments were carried out on tidal flats at Balgzand (A) in the westernmost part of the Wadden Sea in 1990 and near the island of Schiermonnikoog (B) in 1992 (Fig. 1). At these sites a PVC-mat was placed over the sediment during winter. After removal of the mats in March, homogeneous, depopulated (azoic) squares of -100 m2 were obtained. Within these squares, small plots of 1 m 2 each were restocked with four different densities of A. marina (25, 50, 75 and 100 per m2) and C. edule (250, 500, 750 and 1000 cockles of 2 cm length per m2). In the square at Balgzand also three different densities of A.
COROPHIUMARENARIUM IN THE DUTCH WADDEN SEA
marina plus C. edule (12 lugworms + 125 cockles, 25 + 250 and 50 + 500 per m 2) were stocked in the small plots. The animals were collected at nearby tidal flats and transported to the plots as fast as possible. The restocking was done two weeks after removal of the mat in which time an oxygenated top layer had developed in the sediment. All densities were applied in duplicate and there were empty spaces of 50 cm width between the small plots to avoid interactions. Three of these small plots remained empty to serve as controls. On the tidal flat near the island of Schiermonnikoog
283
the densities of cockles and lugworms were also manipulated in the otherwise undisturbed natural situation. The naturally occurring densities of these species were estimated first, after which these densities were augmented in small plots of 1.5 x 1.5 m to reach densities of A. marina of 50, 75 and100 per m 2 and of C. edule of 500, 750 and 1000 per m 2. All densities were applied in duplicate, the natural situation around these plots was used as a control. In three small plots the numbers of A. marina were diminished by stabbing the lugworms to death with thin pins, which resulted in densities of ~10 per m 2 (natural densities
TABLE 1 The sediment composition along various transects of ~1 km from the shore to the tidal channel in different parts in the Dutch Wadden Sea and the Corophium species and densitiy found at that place. (No. 1 is close to the shore, no. 10 (Balgzand 20) is the middle of the transect and no. 20 (Balgzand 40) is the end of the transect. Not all transects were this long: Noordsvaarcler, Koffieboonplaat and Den Oever were only 300 m). Place
Den Oever Balgzand
No
% silt (<50 IJ.m)
1
med. grain size (m)
muddy
Corophium sp. C. volutator
n per m2
45412
1 20 40
11.2 3.5 1.1
141.7 157.3 175.9
C. volutator no Corophium C. arenarium
510
Texel
1 10 20
24.8 1.8 1.1
90.6 176.9 178.0
C. volutator C. arenarium C. arenarium
78 550 745
Vlieland
1 10 20
12.3 5.2 2.2
184.4 182.6 137.9
algae cover C. arenarium no Corophium
78
1 10 20 1 1
18.4 4.6 1.3 1.2 1.1
161.7 189.4 184.8 209.6 216.7
C. volutator C. arenarium C. arenarium C. arenarium C. arenarium
Ameland
1 10 20
4.2 2.5 4.4
184.1 176.1 177.2
C. arenarium C. arenarium no Corophium
157 39
Holwerd
1 10
28.8 4.0
75.4 110.4
C. volutator C. arenarium
39 78
Schiermonnikoog
1 10 20
2.9 2.5 1.3
169.8 169.9 170.0
C. arenarium C. arenarium no Corophium
1843 274
Hornhuizen
1 10
C. arenarium C. arenarium
78 235
Noordpolderzijl
1 10 20
Terschelling
Noordsvaarder Koffieboonplaat
rather sandy rather sandy 75.1 19.2 4.1
33.3 90.3 114.4
C. volutator C. volutator no Corophium
120
2862 510 157 470 1137
62471 28941
284
E.C. FLACH
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ence of the two Corophium species. The first experiment was carried out in three aquaria (A, B and C) of 40 x 20 x 30 cm (I x w x h), filled with a layer of 15 cm sieved sandy sediment. Partitions of 20 cm height were placed in the sediment halfway the length of the aquaria. The aquaria were filled with filtered sea water to the upper edge of the partitions (-5 cm). At the right-hand side of aquarium C, 15 C. edule of -3 cm length (-12% coverage) were placed, at that of aquarium B 4 A. marina (-100 per m2), whereas the right-hand side of aquarium A remained empty. The left-hand side was kept empty in all aquaria. Twenty C. arenarium (-500 per m 2) were released at the right-hand side of the aquaria, where they were first allowed to settle. After -24 h the water level was raised to ~10 cm above the partition, enabling C. arenarium to swim freely to the left-hand side. The aquaria were placed in a row with the light from above and they were aerated in the middle of the aquarium. After two weeks the numbers of C. arenarium at the two sides of the partition were counted. This experiment was repeated 14 times. The Wilcoxon-MannWhitney test (SIEGEL& CASTELLAN, 1988) was used to test whether the numbers of migrated Corophium were different in the aquaria with cockles or lugworms as compared to the 'empty' control aquarium. The second type of experiment was performed in two aquaria of 40 x 10 x 30 cm in which two partitions of 10 cm height were placed to obtain three equally sized compartments. These compartments were filled with three different types of sieved sediment: a silty sediment (from a place where high densities of C. volutatorwere found), a sandy sediment and a mixed sediment composed of the two other types. The arrangement of the sediment types differed in the two aquaria. The aquaria were placed next to each other with the light from above and they were aerated in the middle of the aquarium. The aquaria were filled up with a layer of 15 cm filtered sea water, and 20 C. arenarium or C. volutatorwere released in the water column, so that they could settle freely in any of the three sediment types. After two weeks the numbers of Corophium in each of the three compartments were counted. This experiment was repeated 15 times and
-30 per m2). All plots were sampled once in early July and once at the end of August. From each plot three samples were taken of 255 cm 2 each to a depth of -10 cm. These samples were treated as described above for the surveys. At the time of sampling the number of lugworm castings in the plots was counted as well, and also the numbers of cockles in the samples. The 35C0 length of the cockles was measured to calculate the 3ooo area fraction covered by the cockles as described by 250O JENSEN(1985). A non-parametric trend-test, which is a modification "E 20oo of the Kruskal & Wallis test, described by DE JONGE c 1500(1963: p. 340), was used to evaluate the effects of the IOOO" densities of cockles and lugworms. A short descrip5OOtion of this rank test is given by BEUKEMA(1968: p. 9). o
2.3. LABORATORY EXPERIMENTS Two kinds of laboratory experiments were carried out, one to study effects of cockles and lugworms on C. arenarium and the other to study the sediment prefer-
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along a transect from the shore (no. 1) to the tidal channel (no. 20) near the island of Terschelling, July 1992. Distance
between the samples is - 50 m.
COROPHIUM ARENARIUM IN THE DUTCH WADDEN SEA
the sign test (SIEGEL& CASTELLAN, 1988) was used to test whether the numbers of settled Corophium were different between different sediments offered.
285
C. a c e n a d u m n per m*
60
50'
3. RESULTS
40
3.1. SURVEYS
30 20
Fig. 1 shows the spots where Corophium was sampled during the survey of July 1992 in the Dutch Wadden Sea. At most tidal-flat stations C. arenarium was found in low densities; C. volutator was found only in a few places, though then mostly in high densities. If C. volutatorwas found, it was invariably at the highest places close to the shore in muddy sediments, whereas C. arenarium was found in sandy sediments only (Table 1). These sandier parts are mostly also the lower parts of the tidal flats at which also rather high densities of A. marina and C. edule can be found. Fig. 2 gives an example of the distribution of the two Corophium species, and of lugworms and cockles along a transect at Balgzand from the shore (high-tide level, no. 1) to the tidal-channel (low-tide level). Elsewhere the two species occurred in the same zone (Fig. 3). At two places relatively high densities of C. arenarium were found, viz. on the Koffieboonenplaat at the eastern part of Terschelling and at a tidal flat near Schiermonnikoog. In these areas, the highest densities were found at high levels close to the shore (Fig. 4), which had unusually sandy sediments for such high intertidal levels (Table 1). Fig. 4 also shows that the densities of C. arenarium along their transect were negatively related to the densities of A. marina (Spearman rank-correlation coefficient r= -0.73, p
50
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~ . - ~-- ~r.~ 1
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=
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Fig. 4. Distribution patterns of A. marina and C, arenarium along a transect from the shore (no. 1) to the tidal channel (no. 20) near the island of Schiermonnikoog, July 1991. Distance between the samples is -50 m.
10 0
, 200
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i
t
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Fig. 5. Relationships observed in square A between the densities (n.m-2) of C. arenarium and actual densities at the time of sampling (July 1990) of (a) C. edule (R = -0.62, p
286
E.C. FLACH
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August is given in Fig. 7b. In the otherwise undisturbed natural plots, in which only the densities of cockles and lugworms were manipulated, only the effect of the removal of lugworms was significant (13<0.01) in July (Fig. 6b). In the three small plots from which only the lugworms had been removed, the densities of C. arenarium were about 10x higher than in the natural situation. These high densities were similar to those found in the empty plots of the defaunated square. Fig. 8 shows the relationship between the actual densities of A. marina and the C. arenarium densities in all natural plots in August. Although the lugworm densities were different in the cockle plots, the densities of C. arenarium were about equally low in all cockle plots (area fraction covered by C. edule between 12 18%). Although there were strong differences in total numbers, the population structures of C. arenarium
,,5 1 0 o o .
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Fig. 6. The mean densities (n.m-2 with one standard error) of C C. arenarium (a) in the small plots within the defaunated E 6OO, square populated with different initial densities of A. marina _= and C. edule (number of replicates n=2) compared to the f~ 4OO empty (azoic) plots (n=3) and (b) in otherwise undisturbed 9o 20O plots with additions of Arenicola (At.+) and Cerastoderma u (Cer.+) (n=6) and removal of Arenicola (Ar.-) (n--3) of these species compared to the fully natural situation (nat.) (n=6). 0 All observations made at site B near the island of Schiermonnikoog, July 1992.
!
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40
50
Arenlcola
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the natural situation around the square. A strongly 1200 b negative effect of the presence of A. marina was found. Their initial approximately natural density of 25 ~ looo had diminished to N18 lugworms per m 2 and even this low density caused a reduction of N50% in C. are- ~ 800 narium densities. The initial enhanced densities of 50, C 75 and 100 lugworms had diminished to 40, 46 and E 600 43, respectively, in July, causing the numbers of C. arenarium to be about equal in these plots (Fig. 6a). } 4oo In these lugworm plots the densities of C. arenarium 0 were about the same as in the natural situation (-30 u 20O lugworms per m2). With the actual lugworm densities, | 13 a significant density-dependent negative effect on the 0 5 10 15 densities of C. arenarium was found (p<0.01, trend% occ. by Cerast. test). A negative relationship between the actual lugworm densities present in the small plots and the densities of C. arenarium was also found in August Fig. 7. The densities (n-m-2) of C. arenarium in the small (Fig. 7a). Also a significant (p<0.05, trend-test) nega- plots within the defaunated square stocked with different initive density-dependent effect was found of C. edule tial densities of A. marina (a) and C. edule (b). Given are the on the numbers of C. arenarium, although the lowest actual densities of A. marina and the actual % of area covdensity (250 cockles with ~1.1% area coverage) did ered by C.edule at site B in August. The % area coverage of not differ from the empty plots (Fig. 6a). The relation- C. edule was calculated after JENSEN (1985) by counting ship between the actual proportion of area coverage and measuring the cockles from each plot. The numbers of by C. edule and the numbers of C. arenarium in A. marina were estimated by counting the castings•
COROPHIUM ARENARIUM IN THE DUTCH WADDEN SEA
nificantly higher numbers of C. volutator settled in the silty sediment as compared to the sandy sediment (p
1000 800
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4. DISCUSSION
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80
n por m 2
Fig. 8. The densities (n.m-2) of C. arenarium related to the densities of A. marina in the small plots with additions of A. marina (At) and C. edule (Cer) and from which A. marina (Ar) was removed in the otherwise undisturbed natural situation compared to the fully undisturbed natural situation (nat) at site B in August 1992. were similar in all plots. Neither was there any significant difference in the number of eggs per female between the different treatments. The number of eggs per female were in most cases rather low (<15 per female), and the mean number of eggs per female was only 4.7 + 2.4 (n = 92). This low number was partly due to the small size of most egg-bearing females (mean length 4.5 + 0.8), but even most of the larger females had few eggs. No correlation between the number of eggs and the developmental stage was found, which suggests that no significant loss of eggs occurred during the period of development.
The results of the field experiments, viz. strongly negative effects of both C. edule and A. marina on the ')undance of C. arenarium, were similar to the suits obtained in previous experiments in C. volutar (FLACH, 1992). In the case of C. volutator, however, e experimental results could quite well explain the ;neral distribution patterns found in the Wadden _ ;a with C. volutatoras the dominating species in the upper tidal zone and C. edule and A. marina dominating the bordering lower intertidal zone. C. arenarium, however, was frequently found in the highest numbers exactly in this lower A. marina + C. edule dominated zone (as exemplified in Fig. 2). This raises a problem, because the abundance of both C. volutator and C. arenarium was found to be affected negatively by the presence of A. marina and C. edule (and in the case of A. marina already at low numbers of this species). JENSEN & KRISTENSEN (1990) explain the differential zonation of the two Corophium species by the competitive superiority of C. volutator over C. arenarium. C. volutator inhabits the upper part of the intertidal zone, probably restricted to it by factors such as the presence of lugworms in the lower zone, leaving the lower zone to C. arenarium. These authors did not find any significant differences in abiotic factors 10
3.3. LABORATORY EXPERIMENTS Fig. 9 summarizes the result of the experiment on the effect of the presence of cockles and lugworms on the distribution of C. arenarium. Significantly (p
9 8
7 I=1
~ 2
6 5
,-
4 3 2 1 0
o
empty
I Arenlc.
I Cerast.
Fig. 9. The mean number (with standard error) of C. arenarium that had migrated in the aquaria with A. marina or C. edule compared to the aquarium without the latter two species (empty). The experimentwas replicated 14 times.
288
E.C. FLACH
between the two places (with rather sandy sediments) where they found the two Corophium species. In the Dutch Wadden Sea, however, C. volutatorwas found to be restricted to muddy sediments and C. arenarium to sandy sediments (Table 1), with little overlap: such differences were also found by WATKIN (1941) in the Dovey Estuary. The aquarium experiments also suggested that C. arenarium prefers sandy sediments and C. volutator muddy sediments (Fig. 10). The composition of the sediments in which JENSEN& KRISTENSEN(1990) observed the two species was similar to those in which only C. arenarium was found in the Dutch Wadden Sea. Along the two transects (Schiermonnikoog, Koffieboonenplaat) with only sandy sediments (even at the higher parts), only C. arenarium was found. In these two areas, the densities of C. arenarium were particularly high in the higher parts. This agrees with the results of the field experiments as the densities of both A. marina and C. edule were low in these higher parts. Removal of lugworms caused -lOx higher C. arenarium densities both in the natural situation and in the defaunated square, whereas these densities were at the same level as in the natural situation in the plots with high lugworm densities. So, it can be concluded that the low natural density must have been due to the presence of A. marina. This was also suggested by the mirrored pattern of densities of lugworm and C. arenarium along the Schiermonnikoog transect (Fig. 4). The strongly negative effect of cockles on the abundance of C. arenarium could not be compared to a natural situation because only low natural cockle densities (-1-2% area coverage) were found. However, the results of the experiments suggest that high cockle densities would further reduce the numbers of C. arenarium (Fig, 8). Although the densities of C. arenarium were much higher in the upper parts of the transects at Koffieboonenplaat and Schiermonnikoog and in the experimental lugworm-free plots than in any place where lugworms were present, maximal densities of C. arenaria were far below the maximal densities of C. volutator. This difference between the two species can be explained by the much lower reproductive capacity of C. arenarium (FISH& MILLS, 1979; JENSEN& KRISTENSEN, 1990). The mean number of eggs per female (-4.7) at a mean length of the females of -4.5 mm found in this study was even lower than that reported by FISH & MILLS (1979), viz. ~12.8 eggs at a female length of 4.7 mm in July. FISH& MILLS(1979) also report a difference in egg number at stages 1 and 4, indicating a loss from the broodpouch of -26%. Such a loss was not found in the present study. Neither did I find any difference in eggnumber between the different treatments, whereas for C. volutator somewhat lower eggnumbers were found in treatments with high cockle or lugworm densities (FLACH, 1993). The effect of cockles and lugworms on the C. volutator population structure (viz. a lower proportion of gravid females and smaller
50 40 .E ~ 30 • o d 20 10
m
0.30%
5.30%
207,9 IJ
198,7 ~J
0 sand
mixed
silt
60 m
50
r
~ 40 ~ 30 d
~ 20 1o 0
I
sand
I
mixed
I
silt
Fig. 10. The mean proportion (with standard error) of (top) C. arenarium and (bottom) C. volutatorthat settled in the different sediments in the sediment-choice aquaria. The sediment composition is given in the bars, upper number is % silt (<50 p.m), lower number is median grain size (in #m). The experiments were replicated 15 times. sizes (FLACH, 1993)) was not found in C. arenarium. However in C. volutator, it were especially the bigger individuals (>5.5 mm) that were affected; in C. arenarium such sizes were not found. The results from the aquarium experiments suggest that the negative influences of lugworms and cockles were not caused by a higher in situ mortality rate but rather by a higher migration rate in C. arenarium. This migration was probably induced by the sediment-disturbing activities of lugworms and cockles. A. marina is known for its high bioturbation rate, especially in summer with a daily average of sediment reworking of -27.7 cm 2 per worm (CADI~E,1976). Already at intermediate lugworm densities (-17 per m 2, the mean for the tidal flats of the Wadden Sea
COROPHIUM ARENARIUM IN THE DUTCH WADDEN SEA
289
(BEUKEMA & DE VLAS, 1979)) this activity can cause a work in the nature reserve Schiermonnikoog. And I would severe disturbance of the upper sediment layer. LINKE also like to thank W.J. Wolff and two anonymous referees (1939) already suggested that this sediment-rework- for their useful comments on an earlier version of the manuing activity of A. marina could have negative effects script. on the tube building C. volutator. BREY (1991) con5. REFERENCES cludes that especially the funnels of A. marina cause a strong reduction in number of C. volutator. It is likely BEUKEMA,JJ., 1968. Predation by the three-spined sticklethat the same would apply to the closely related C. back (Gasterosteus aculeatus L.): The influence of arenarium. JENSEN (1985) reports that the burrowing hunger and experience.--Behaviour 31:1-126. and ploughing habits of C. edule negatively affect C. BEUKEMA,J.J. & J. DE VLAS, 1979. Population parameters of volutator. He found high migration rates at high cockle the lugworm Arenicola marina, living on the tidal flats of the Dutch Wadden Sea.--Neth. J. Sea Res. 13" 331densities, but also low in situ survival, growth and 353. reproduction. In the present study, however, only higher migration rates were found at high cockle den- 8REY, T., 1991. The relative significance of biological and physical disturbance: an example from intertidal and sities; no effects on survival or reproduction of C. aresubtidal sandy bottom communities.--Estuar, coast. narium were found. This negative effect resulted not Shelf Sci. 33: 339-360. merely from the presence of cockles as can be seen CADI~E,G.C., 1976. Sediment reworking by Arenicola marina from the relationship between the area fraction covon tidal flats in the Dutch Wadden Sea.--Neth. J. Sea ered by C. edule and the reduction in Co arenarium Res. 10: 440-460. numbers. A reduction in C. arenarium numbers of DANKERS, N. & J.J. BEUKEMA, 1983. Distributional patterns of macrozoobenthic species in relation to some environ- 5 0 % was already found at an area fraction covered mental factors. In: W.J. WOLFF. Ecology of the Wadden by cockles of only 5%, and a reduction of ~80% at Sea. Balkema, Rotterdam, Vol. 1, part 4:69-103. 10% coverage of cockles. This reduction was even stronger than that found previously for C. volutator DE JONGE,H., 1963. Inleiding tot de Medische Statistiek. Verhandelingen van het Nederlands Instituut voor Praewhen a reduction of N50% was reached only at ~13% ventieve Geneeskunde, XLI. Leiden, Deel 1, 2e druk: coverage of cockles (FLACH, 1992). The gravity of the 1-421. influence of A. marina was similar in the two FISH, J.D. & A. MILLS, 1979. The reproductive biology of Corophium species, a reduction of ~50% at lugworm Corophium volutator and C. arenarium (Crustacea: densities of N18 per m 2. On the sandy tidal flats of the Amphipoda).--J. mar. biol. Ass. U.K. 5g: 355-368. German Wadden, REISE (1985) found a mean density FLACH, E.C., 1992. The influence of four macrozoobenthic species on the abundance of the amphipod Corophium of no less than ~40 lugworms per m 2. Such a high volutator on tidal flats of the Wadden Sea.--Neth. J. density reduced C. arenarium numbers in the present Sea Res. 2g- 379-394. study to - 1 0 % of those in areas without lugworms. --, 1993. Effects of Arenicola marina and Cerastoderma In conclusion, C. arenarium prefers a sandy sediedule on distribution, abundance and population strucment. In the Wadden Sea, such sediment is most freture of Corophium volutator in the Gullmarsfjord (SW quently present at the lower parts of the tidal flats. Sweden).--Sarsia 78 (in press). Here densities of lugworms and sometimes also JENSEN, K.T., 1985. The presence of the bivalve Cerastocockles are high too. Both cockles and lugworms derma edule affects migration, survival and reproduction of the amphipod Corophium volutator.--Mar. Ecol. have a strongly negative impact on densities of C. Prog. Ser. 25: 269-277. arenarium. This negative effect is probably caused by sediment-disturbing activities of cockles and lug- JENSEN, K.T. & L.D. KRISTENSEN, 1990. A field experiment on competition between Corophium volutator (Pallas) and worms which force C. arenarium to migrate. RelaCorophium arenarium Crawford (Crustacea: Amphiptively high densities of C. arenarium were found only eda): effects on survival, reproduction and recruitat specific places in the Dutch Wadden Sea, characment.--J, exp. mar. Biol. Ecol. 137: 1-24. terized by high intertidal levels (causing low densities LINKE, 0., 1939. Die Biota des Jadebusenwattes.--Helgoof lugworms and cockles) and a sandy sediment lander wiss. Meeresunters. 1: 201-348. (excluding competition by the related C. volutator). OLAFSSON, E.B. & L.-E. PERSSON, 1986. The interaction between Nereis diversicolor O.F. MUller and Thus, the generally low densities of C. arenarium Corophium volutator Pallas as a structuring force in a observed in nearly all of the Wadden Sea will be shallow brackish sediment.--& exp. mar. Biol. Ecol. caused by the presence of lugworms and cockles in 103" 103-117. far most of the (prevailing) sandy sediments. REISE, K., 1978. Experiments on epibenthic predation in the Wadden Sea.--HelgolAnder wiss. Meeresunters. 31: Acknowledgements.--I am grateful to J.J. Beukema for the 55-101. support received during this study. I would also like to thank , 1985. Tidal flat ecology. An experimental approach to E. Adriaans, C. Baltus, W. de Bruin and J. Zuidewind for species interactions. Ecological studies 54. Springer their assistance with the field work and the crew of the RV Verlag, Berlin: 1-191. 'Navicula' for the pleasant trips to the tidal fiats. The Society for the Protection of Nature Reserves, the Ministry of Agri- RONN, C., E. BONSDORFF& W.G. NELSON, 1988. Predation as a mechanism of interference within infauna in shallow culture, Nature Management and Fisheries and the Municibrackish water soft bottoms; experiments with an infaupality of Schiermonnikoog were so kind as to allow me to
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nal predator, Nereis diversicolor O.F. MOIler.~. exp. Mar. Biol. Ecol. 116" 143-157. SIEGEL, S. & N.J. CASTELLANJr., 1988. Nonparametric statistics for the behavioral sciences. 2nd Ed. McGraw-Hill Book Co., Singapore: 1-399. STOCK,J.H., 1952. Some notes on taxonomy, the distribution and the ecology of four species of the amphipod genus Corophium (Crustacea, Malacostraca).--Beaufortia, Amsterdam 21: 1-10.
THAMDRUP,H.M., 1935. Beitr&ge zur Okologie der Wattenfauna auf experimenteller Grundlage.--Meddr Kommn Danm. Fisk.-og Havsunders., Ser. Fisk. 10" 1-125. WATKIN, E.E., 1941. The yearly life cycle of the amphipod Corophium volutator.--J, animal Ecology 10: 77-93. (accepted 10 September 1993)