The macrozoobenthos of the subtidal western dutch wadden sea. I. Biomass and species richness

57

Netherlands Journal of Sea Research 23 (I): 57-68 (1989)

THE MACROZOOBENTHOS OF THE SUBTIDAL WESTERN DUTCH WADDEN SEA. I. BIOMASS AND SPECIES RICHNESS

R. DEKKER 1 Reseamhlnstitute ~ r N a t u ~ Management, P.O. B o x 5 9 , 1 ~ O A B

ABSTRACT During a one-year period in 1981-1982, a survey was conducted on the macrozoobenthos of the subtidal areas of the western half of the Dutch Wadden Sea. In total 80 species were found, half of them polychaetes. In terms of biomass, Mytilus edulis dominated the macrozoobenthos, with Hy-

drobia ulvae, Heteromastus fififormis, Carcinus maenas and Macoma balthica as other important species. Numerically important were also the polychaetes Pygospio elegans and Scoloplos armiger. Average macrozoobenthic biomass amounted to 43.7 g.m - 2 ash-free dryweight. This value is in the same range as values from intertidal areas in the Wadden Sea. The relatively high value in comparison with data from similar subtidal areas is attributed to the important mussel culture in the area. 1. INTRODUCTION The soft-bottom macrofauna of the Wadden Sea has been a subject of quantitative studies for some decades (for a review, see DANKERS et al., 1983). Estimates of production and energy flow in the Wadden Sea ecosystem are based on such studies (BEUKEMA, 1983; KUIPERS et al., 1981; DE WILDE & BEUKEMA, 1984). Most of the studies have been carried out in the intertidal. Among the subtidal studies, the majority were focussed on numerical and distribution aspects only ( DITTMER, 1983). The morphology of the Wadden Sea is far from uniform. In most parts more than 50% of the total area is composed of intertidal flats, whereas the subtidal consists only of tidal inlets and gullies characterized by a relatively high tidal amplitude and fast currents. In other parts, particularly the western Dutch Wadden Sea, but also some areas in the northern German and Danish Wadden Sea, considerable parts of the subtidal are very shallow with a depth

DenBu~, ~xel, ~ e N e t h e ~ n ~

between 0 and 2 m below mean low tide level (MLTL), and the area of the intertidal zone is much reduced. In the western Dutch Wadden Sea (Fig. 1) only about 30% of the area consists of tidal flats, and the major part belongs to the up to now poorly studied subtidal area. Especially the benthic fauna of the shallowest subtidal areas has not been studied. In these shallower parts of the subtidal Wadden Sea, higher biomass values of the subtidal macrofauna might be expected as a consequence of the intensified mussel culture (Mytilus edulis L.) in subtidally situated commercial beds since 1950. In recent years a few quantitative studies have been published on biomass of the subtidal softbottom macrofauna in small parts of the Wadden Sea (BEUKEMA, 1977; VAN ARKEL & MULDER, 1979; HAVERKAMP, 1981). These studies, and additional Van Veen grab surveys by the Netherlands Institute for Sea Research (unpubl. data), were carried out in tidal inlets and deep tidal channels. They all showed a poverty in macrofauna compared with intertidal data. From the similarly structured Grevelingen and Oosterschelde estuaries (S.W. Netherlands) data on subtidal macrobenthos are also available ( WOLFF, 1973; WOLFF & DE WOLF, 1977; FORTUIN, 1981; COOSEN & VAN DEN DOOL, 1983). AS far as they provide biomass data, these studies too show reduced macrozoobenthic biomass values for subtidal stations. This study presents an estimate of numbers and biomass of macrozoobenthos in the subtidal western Dutch Wadden Sea, with the main interest focussed on the shallower parts. It was carried out within the framework of a study project on sedimentology, macrozoobenthos and their relationships in the shallow subtidal western Dutch Wadden Sea. This project was carried out in cooperation between the Ministry of Transport and Public Works, the Netherlands Institute for Sea Research, the State Institute for Fisheries Research and the Research Institute for Nature Management.

IPresent address: Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands.

58

R. DEKKER

2. DESCRIPTION OF THE AREA

Acknowledgements.--I am grateful to J.J. Beukema, K. Essink, G.W.N.M. van Moorsel and A. de Gee for stimulating discussions and reading of the manuscript. The IJsselmeer Polders Development Authority constructed the flushing sampler and put it at my disposal during the sampling programme. M.A. van Arkel and M. Mutder gave advice on the use of the flushing sampler and lent me part of the sampling equipment. J. Zuidewind, W. de Bruin, B. Klein and R. van Kruysen assisted with field work and sorting of the samples. W.J. Wolff identified some of the smaller polychaete species. H. Ridderinkhof provided detailed information on the depth distribution of the study area. R. Dapper provided computer programs and assisted with data handling. Acknowledgement is due to the crew of R.V. Navicula, and particularly to skipper C. Wisse, for the guidance on the Wadden Sea, and the pleasant atmosphere on board.

--

|

Terschellingi

-~i

%'-..

i; '

2.1. MORPHOLOGY AND SEDIMENTS The survey covered the subtidal parts of the western Wadden Sea, i.e. west of the tidal watershed between the island of Terschelling and the mainland, except for the subtidal areas connected with the small tidal inlet between the islands of Texel and Vlieland (Fig. 1). Near the tidal inlets the area is characterized by strong tidal currents and relatively high water turbulence. Salinity of the water is fairly constant and nearly equal to that of the adjacent North Sea (S = 30). Near the mainland weaker tidal currents and low water turbulence prevail. Salinity of the water shows strong fluctuations (S= 10 to 34) due to freshwater discharges at several places along the coast, especially through the sluices in the "Af-

~

\..

,Griend

]~,;

;W< -"~

~%Z~-"

i

/ I

1

i'

,. ;

,'

~

\

L°ke 'U''e'

--'-- Borders of stud)' area

WESTERN DUTCH WADOEN SEA

Fig. 1. Map of the western Dutch Wadden Sea, indicating the locations of the 45 transects of the survey.

ZOOBENTHOS OF SUBTIDAL WADDEN SEA

sluitdijk", the dam separating the Wadden Sea from the freshwater Lake IJssel. The mean tidal amplitude in the westernmost part of the study area is 1.36 m, and increases up to 1.80 m near Terschelling. In the study area the intertidal area is much reduced ( - 2 0 % of the total of - 1 4 0 0 km2), and relatively vast shallow subtidal areas of approximately constant depth (so-called subtidal flats) cover a considerable part ( - 5 0 % , Table 1) of the total area (Fig. 2). These subtidal flats, between MLTL and MLTL 2 m, are bordered by gullies, tidal flats and dikes. The bottom of the area consists of soft sediments. In the tidal gullies medium sands mixed with shells and shell fragments prevail. Locally, coarser sands, gravel and even stones are present. Pleistocene boulder-clay and early Holocene clay and peat layers may come to the surface on the sides of deep gullies. The subtidal flats generally consist of finer and siltier sediments than those of the gullies. However, a high variation is found in the sediment characteristics of the subtidal flats as a consequence of local differences in hydrodynamical conditions. Especially silt contents are highly variable, and range from nearly 0 in areas near tidal inlets, to over 25% locally -

59

nearshore (ENTE, 1987). The sediments under the mussel beds generally have the same sedimentological characteristics as the surrounding seafioor. On this sediment mussels deposit pseudo-faeces, providing it with a toplayer of almost pure silt (DANKERS, 1986). 2.2. MUSSEL CULTURE At present, about 7% of the subtidal area is in use for mussel culture (Fig. 3). It is mainly restricted to areas between MLTL and MLTL - 3 m, although during the survey mussel culture plots were found down to - 7 . 5 m. The culture plots have fixed positions through the years, but are not permanently occupied with mussels. Mussel farmers stock their culture plots with mainly 0-group mussels with a shell-length of - 1.5 to 2 cm. These so-called "seed-mussels" are collected from both intertidal and subtidal wild banks. During their ca. 2 years on the plots the mussels are regularly fished up for removal of predators (mainly Asterias rubens L.) and redistribution on the plots in optimal densities. 3. MATERIALS AND METHODS

Surface ere(] x I06 m2 O "I" MLTLO" -2' MHTL

200

400

600

800

I000 1200 1400

i

-IO.

-15-

Between September 1981 and July 1982 a total of 457 stations were sampled along 45 transects scattered over the entire area. Most transects were situated perpendicular to the direction of the tidal channels (Fig. 1). Most attention was paid to the area between MLTL and MLTL - 4 m , 380 stations being situated within this depth range (Table 1). 35 Stations (7.5%) were located in mussel culture plots. All stations were sampled once. At each station also environmental data such as depth and sediment characteristics were collected. These data will be used in a later paper.

-20-

-25.

-30-

-35"

depth (m) Fig. 2. Diagram showing the depth-surface area relationship in the surveyed part of the western Dutch Wadden Sea (after H. Ridderinkhof, pers. comm.).

TABLE 1 Subdivision of the study area into depth zones with corresponding surface areas (H. Ridderinkhof, pers. comm.), numbers of samples per depth interval and conversion factors for numbers and biomass data. Depth interval (m) Area (in km2) Number of Conversion (related to ML TL) samples factor 0.0 to 2.0 - 2.0 to - 4.0 -4.0 to - 10.0 under - 10.0

677.25 178.50 158.25 98.25

287 94 58 18

total subtidal intertidal

1112.25 301.25

457

total area

1413.50

0.970 0.780 1.121 2.243

60

R. DEKKER

=

-~..

f ,

__

\.\

',,%:,

_

i ,'>--' ,, .-


.

_-;°.-

/-..

- - ~

- ",'-'."

-

_

-

"--

-,

,-/

.}

,..;-.~.-

/~P

~

/ ~ - ~ , . " { i:'~', /,"' ' " ' " ~ 1 i ~ -; ,' ~ \ B.Qrgzond f ~ . / ~

.... Lake IOssel \ \

I S \

=~ .-. . . . . . . ~ ....

=

Main fresh=.ater discharge Borders of study area

WESTERN DUTCH WADDEN SEA Mussel cuture lots

Fig. 3. Map of the western Dutch Wadden Sea, with isobaths and indicating the locations of the mussel culture plots present in 1981/1982 (source: Ministry of Agriculture and Fisheries). Two types of bottom samplers were used: a 0.2 m 2 Van Veen grab and a 0.2 m 2 flushing sampler (VAN ARKEL & MULDER, 1975) modified for subtidal sampling from a large vessel. The Van Veen grab is relatively small and easy to handle, but the efficiency of this sampler is dependent of the sediment type. The maximum sampling depth is generally limited to - 8 to 10 cm ( BEUKEMA, 1974a), so deep-living species will nearly always be missed. Thus, for proper quantitative sampling this grab is not sufficient. The Van Arkel flushing sampler (Fig. 4) can penetrate much deeper. For a description of the sampler and operation details see VAN ARKEL & MULDER (1975). The penetration depth is adjustable. Because in the Wadden Sea and adjacent shallow subtidal areas macrobenthic infauna seldom lives deeper than - 3 0 cm under the sediment surface (BEUKEMA, 1974a, 1974b), the flushing sampler was adjusted to a depth of 40 cm. The major disadvantage of this version of the Van Arkel flushing sampler, however, is its inability to penetrate into sediments with a high proportion of big shells (e.g. Mya arenaria L.), into firm sediments like peat and tough clay, and into mussel beds,

where the shells are firmly attached to each other by byssus-threads. Another disadvantage is the limited length of the hose connecting the vessel-based water pump to the sampler. As a consequence, only sediments at bottoms less than - 5 m deep could be sampled with the flushing sampler. Thirdly, the flushing sampler was constructed after the original design by VAN ARKEL & MULDER (1975), which was not able to sample the heaviest molluscs, i.e. Cerastoderma edule (L.) and adult Macoma balthica (L.) (DEKKER, 1982). An improvement of the design (MULDER & VAN ARKEL, 1980) was not applied to the flushing sampler used during this survey. Therefore, both samplers were used at each station whenever possible. Per station, 3 samples with the flushing sampler, pooled to one sample of 0.06 m 2, and one Van Veen-grab sample (0.02 m 2) were taken, the latter providing both additional information on heavy bivalves and larger epifauna and a sediment sample. For 75 stations (16%) only a Van Veen-grab sample could be obtained, and so a possibly less complete picture of the benthic macrofauna.

ZOOBENTHOS OF SUBTIDAL WADDEN SEA

61

iilJJiitliJiiJiKJiilJiiliiiiJiiJJiJiiiJiJ [ 1

<

Fig. 4. Flushing sampler used during the survey. (left) Schematic view. 1: hose connection; 2:1 mm sieve basket; 3: valve. (right) Mounted in a frame, at the moment of lowering to the sea bottom. For a detailed operation description see MULDER & VAN ARKEL(1980) and DEKKER(1982). The material retained in the 1 mm gauze basket of the flushing sampler was stored in 10% formalin. After a small subsample for sediment analysis had been taken, the Van Veen grab material was sieved on board and the retained material deep-frozen. Only at stations without a flushing sample was the retained material of the Van Veen-grab sample stored in 10% formalin. In the laboratory the samples were sorted to species level. The polychaetes were not removed from the deep frozen Van Veen-grab samples, as they were generally too much damaged after freezing to allow proper identification and biomass determination. The bivalves were sorted into year-classes. The determination of the ash-free dry weight (AFDW), an indicator for biomass, was carried out according to BEUKEMA (1974b). For biomass deter-

mination of the bivalves only the soft parts were used. The brown shrimp (Crangon crangon (L.)) was excluded from the analyses, because of its mobility and ability to escape from approaching samplers (BEUKEMA, 1974a). To compare biomass data from different periods of the year, the data were converted to annual averages according to the seasonal curve of the macrobenthic biomass as observed in the intertidal (BEUKEMA, 1974b). Per date the same conversion factor was used for all species (Table 2). The sampling programme was not developed as a stratified random programme. Therefore, the data for biomass and numbers were corrected for over or underrepresentation of the various depth zones. The correction factor for each depth interval is given in Table 1.

62

R. DEKKER

TABLE 2 Conversion factors (used to convert observed biomass values to annual averages) derived from BEUKEMA(1974b: p. 100). n.s. = not sampled. January February March April May June

n.s. 1.45 1.45 n.s. n.s. 0.81

July August September October November December

0.77 n.s. 0.89 1.02 1.17 1.31

Compared with the most recent species list (WOLFF & DANKERS, 1983), the following species are new to the Dutch part of the Wadden Sea: Harmothoe sarsi (Kinberg), Microphthalmus similis Bobretzky, Nephtys cirrosa Ehlers, Nephtys caeca (Fabricius), Aricidea minuta Southward, Paraonis fulgens (Levinsen), Scolelepis bonnieri (Mesnil), Gastrosaccus sanctus (Van Beneden), Diastylis bradyi Norman and Urothoe guilliamsoniana (Bate). Urothoe elegans (Bate) is new to the entire Wadden Sea. 4.2. NUMERICAL DENSITIES AND FREQUENCY OF OCCURRENCE

4. RESULTS 4.1. SPECIES COMPOSITION During the survey, a total of 80 macrobenthic species was found (Appendix). In terms of species richness the subtidal western Dutch Wadden Sea was dominated by polychaetes: they formed nearly half of the total number of species (38). Other important groups were crustaceans (21 species) and molluscs (15 species). The majority of the species belonged to the shallow infauna and were deposit feeders or carnivores.

Among the 15 most abundant species (i.e. >10 m-2), 10 were polychaetes and 4 were molluscs (Table 3). As to total numbers, Hydrobia ulvae (Pennant) dominated by far, accounting for no less than 88% of the macrozoobenthic numbers. The most frequently occurring species was Macoma balthica (at 82% of the stations), followed by the polychaetes Scoloplos armiger (Mtiller) (70%), Heteromastus filiformis (Clapar~de) (55o/o) and Nephtys hombergfi Savigny (50%). 4.3. BIOMASS

TABLE 3 Numerically most abundant macrozoobenthic specie.¢ .1 their frequency of occurrence in the subtidal western uucch Wadden Sea. Densities with 95% confidence limits in brackets. Frequency of occurrence expressed as the percentage of stations (n=457) at which a certain species was present, not corrected for over- or underrepresentation.

Average density (n.m -2) +_c.f.

Frequency of occurrence (%) (rank)

Species

Hydrobia ulvae 12967 ( _+ 5689) Heteromastus filiformis 847 ( + 222) Pygospio elegans 179 (+ 87) Mytilus edulis 120 (+ 66) Scoloplos armiger 103 (+ 14) Oligochaetes 93 (+_ 55) Capitella capitata 62 + 18) Spio filicornis 46 + 21) Magelona papillicornis 43 + 13) Macoma balthica 42 (+ 7) Tharyx marioni 29 + 13) Nephtys hombergii 17 (+ 3) Eteone Ionga 17 (+ 3) Petricola pholadiformis 12 (_+ 18) Spiophanes bombyx 10 (_+ 5) Carcinus maenas 6 (_+ 2) Other species each < 10 All species 14680 (+ 5691)

27 (10) 55 (3) 28 (9) 16 (16) 70 (2) 21 (11) 40 (6) 36 (7) 35 (8) 82 (1) 19 (13) 50 (4) 42 (5) 3 (34) 11 (23) 21 (12) <20 (14 +)

4.3.1. TOTAL BIOMASS Corrected only for seasonal fluctuations, the average biomass of macrozoobenthos of all 457 stations sampled amounted to 43.1 g-m -2 AFDW. Corrected also for over and underrepresentation of the different depth strata the average biomass would be 43.7 g.m -2 AFDW. Table 4 lists the biomass values for the most important macrobenthic species. The paramount importance of the mussel Mytilus edulis is clear (66%). Other important contributors to the biomass (>1 g-m -2 AFDW) were the molluscs Hydrobia ulvae, Macoma balthica and Cerastoderma edule, the polychaete Heteromastus filiformis and the crustacean Carcinus maenas (L.). These 6 species together represented over 90% of the total subtidal macrozoobenthic biomass. Among total biomass, 71% was formed by filter feeders (as defined in the appendix), 22% by deposit feeders, 1% by omnivores and 6% by carnivores; 82% of the total biomass was formed by epifauna, 12O/o belonged to the shallow infauna, while only 6% was formed by deep living species such as Heteromastus filiformis and Mya arenaria. 4.3.2. MUSSEL BEDS

Mytilus was found at only 21 (4.6% of the total of 457 stations) of the 35 (7.5%) stations situated within

ZOOBENTHOS OF SUBTIDAL WADDEN SEA

63

TABLE 4 Biomass (in g.m-2 AFDW) of the most important species of macrozoobenthos in the subtidal western Dutch Wadden Sea, Areas without and within mussel culture plots are separately listed. 95% confidence limits (+) in brackets. All stations

Outside culture plots 422

457

Number of stations

Within culture plots 35

Species Mytilus edulis Hydrobia ulvae Heteromastus fififormis Carcinus maenas Macoma balthica Cerastoderma edule Petricola pholadiformis Mya arenaria Nereis virens Scoloplos armiger Nephtys hombergii Arenicola marina Asterias rubens Lanice conchilega Sagartia troglodytes Nereis succinea Nephtys caeca Magelona papillicornis Other polychaetes Rest Total

28.7 4.9 2.1 1.7 1.4 1.4 0.6 0.4 0.4 0.4 0.4 0.2 0.2 0.1 0.1 0.1 0.1 0.1

(13.6) (1.8) (0.5) (0.7) (0.2) (1.7) (1.1) (0.4) (0.3) (0.1) (0.1) (0.1) (0.1) (0.1) (0.1) (0.1) (<0.1) ( < 0.1 )

0.3 0.1

10.3 5.3 2.2 1.6 1.5 1.5 0.7 0.4 0.4 0.4 0.4 0.2 0.1 0.1 0.1 0.1 0.1 0.1

(7.4) (1.9) (0.6) (0.7) (0.2) (1.9) (1.2) (0.4) (0.3) (0.1) (0.1) (0.1) (0.1) (0.1) (0.1) (0.1) (0.1) ( < 0.1 )

251.1 0.2 1.3 2.8 0.8 0.1 < 0.1 0.4 1.1 0.3 0.5 0.3 1.3 0.4 0.5 0.3 0.0 0.0

0.2 0.1

(157.0) (1.8) (0.8) (1.8) (0.5) (0.5) (0.2) (0.6) (1.0) (0.2) (0.4) (0.3) (1.4) (0.8) (0.4) (0.4) (0.0) (0.0)

0.3 0.4

43.7

(14.2)

25.5

(8.6)

262.1

(156.9)

Feeding groups

Mean biomass

Share (%)

Mean biomass

Share (%)

Mean biomass

Share (%)

Filter feeders Deposit feeders Omnivores Carnivores

31.1 9.4 0.6 2.6

71 22 1 6

12.9 9.8 0.5 2.3

51 38 2 9

249.4 3.5 1.5 5.1

96 1 1 2

mussel culture plots. Nevertheless, total biomass inside culture plots equalled an average of no less than 262.1 g.m -2, whereas it was on average only 25.5 g-m -2 outside these plots (Table 4). The high proportion of Mytilus edulis even outside the culture plots is due to the presence of wild mussel beds, which were found in 9 locations (2%). 4.3.3. DEPTH DISTRIBUTION The biomass of Mytilus edulis was higher in the deeper areas (below - 4 m) than in the shallower areas of the subtidal (Table 5). Some dominant species of the intertidal, e.g. Cerastoderma edule, Mya arenaria and Arenicola marina (L.) (BEUKEMA, 1974b, 1976), were found only in the shallowest parts of the subtidal area. The biomass of deposit feeders tended to decrease with increasing depth, omnivores and carnivores showed a reverse trend: higher biomass values in deeper parts of the subtidal

area, which may be related to the increasing trend in biomass of Mytilus. 5. DISCUSSION Because this survey is the first in the Dutch Wadden Sea covering such a large part of the subtidal area, its results fill a gap in the knowledge of the role of the macrozoobenthos in the Wadden Sea. As a consequence of the use of two samplers, both having their own limitations, deep-living heavy molluscs will have been underrepresented at all stations in the survey. In particular the observed contribution of Mya arenaria will be an underestimate. Deep-living species at 71 (mostly deep) stations will have been missed, as only the Van Veen grab could be used there. On the other hand, at most of these deep stations the sediments were very coarse. Such coarse sediments are generally not preferred by the deep-living species in the Wadden Sea. Hence the

64

R. DEKKER

TABLE 5 Biomass (g.m-2 AFDW) of the macrozoobenthos of the subtidal, subdivided into different depth intervals, and of the intertidal (period 1981-1983, 12 transects on Balgzand tidal flats, after Beukema, pers. comm.). 95% confidence limits (_+) in brackets. subtidal 1981-1982 (this study) Depth range

> 10 m

4-10 m

2-4 rn

0-2 m

intertidal Balgzand 1981-1983

Species Hydrobia ulvae Mytilus edulis Cerastoderma edule Macoma balthica Mya arenaria Nereis spp. Nephtys spp. Scoloplos armiger Heteromastus fififormis Arenicola marina Carcinus maenas Other species Total

0.0 37.3 0.0 0.4 0.0 2.6 0.6 0.0 0.2 0.0 4.3 0.5 45.9

(0.0) (77.6) (0.0) (0.3) (0.0) (5.4) (0.4) (0.0) (0.2) (0.0) (9.0) (92.6)

5.1 41.6 0.0 1.2 0.1 0.6 0.5 0.1 0.7 0.0 3.1 1.7 54.8

(6.6) (53.9) (0.0) (0.7) (0.2) (0.6) (0.2) (<0.1) (0.7) (0.0) (2.0) (55.1)

5.4 21.3 0.1 1.9 0.1 0.2 0.5 0.5 3.7 0.0 1.8 4.0 39.6

(3.2) (23.6) (0.2) (0.6) (0.1) (0.3) (0.2) (0.2) (1.7) (0.0) (1.3) (24.7)

5.4 26.5 2.2 1.5 0.6 0.4 0.5 0.5 2.3 0.3 0.9 0.7 41.8

(2.4) (16.5) (2.9) (0.3) (0.6) (0.3) (0.1) (0.1) (0.7) (0.2) (0.4) (16.8)

0.8 6.7 17.2 4.4 10.8 1.8 0.3 0.6 1.4 6.4 0.7 1.2 52.3

Groups Total filter feeders Total deposit feeders Total omnivores Total carnivores Epifauna Shallow infauna Deep infauna

37.5 0.7 2.6 5.1 42.0 3.7 0.2

42.6 7.5 0.6 4.1 50.5 3.5 0.8

underestimate of the biomass at the deeper stations will be limited. The present survey may be sufficient to obtain a broad overview of the total macrozoobenthos. On the species level, however, it is not necessarily as useful. For species widely dispersed over the entire area, like Macoma balthica, Eteone Ionga (Fabricius), Nephtys hombergfi, Scoloplos armiger etc., the data may provide a reliable picture. This is supported by the narrow confidence limits for both numbers and biomass values in these species. Other species show very clustered distributions, e.g. Mytilus edulis, Petricola pholadiformis Pennant, so the estimates of their densities and biomass are less accurate. Unfortunately, in terms of biomass, Mytilus dominates the macrobenthos by far, so the presented value for total macrozoobenthic biomass in the area is less accurate as well. The results of this survey are based on a single sampling, and therefore the data presented here should be regarded as an incidental picture. In similar areas, processes such as winter mortality, recruitment success etc. are far from constant and result in considerable year-to-year fluctuations in benthic communities (BEUKEMA et al., 1978;

24.7 11.9 0.2 2.8 29.0 6.8 3.9

29.4 10.5 0.4 1.6 33.0 5.6 3.3

34.7 14.6 1.8 1.2 8.5 25.2 18.6

BEUKEMA, 1982; BEUKEMA & ESSINK, 1986; ARNTZ & RUMOHR, 1986). In the intertidal western Dutch Wadden Sea macrobenthic biomass was relatively high in 1981 compared with other years (BEUKEMA & CADI~E, 1986). This may indicate that subtidal macrobenthic biomass during the present survey was somewhat higher than average. For a number of taxa, mainly polychaetes and small crustaceans, biomass values will have been underestimated. Data concerning these species are derived from formalin-preserved samples from the flushing sampler. Preservation in formalin causes decrease in ash-free dry weight of up to 20% in some bivalves, depending on the time the material was stored in the preservative (BREY, 1986). Reliable, quantitative data on the soft-bottom macrofauna, both in the Dutch Wadden Sea and the Delta region, S.W. Netherlands, exist only from the 1960s onwards (WOLFF, 1973; BEUKEMA, 1976; ESSlNK, 1978), but for the Wadden Sea of SchleswigHolstein, Northern Germany, data go back to as early as 1869. In the northern Wadden Sea remarkable changes have occurred over the past century (REISE, 1982; RIESEN & REISE, 1982; REISE & SCHUBERT, 1987). Subtidal macrobenthic communities domi-

ZOOBENTHOS OF SUBTIDAL WADDEN SEA

nated by oysters (Ostrea edulis L.) and reef-building polychaetes (Sabellaria spinulosa Leuckart), common at the turn of the century, had completely disappeared by the 1970s, and were partly replaced in dense mussel beds. Consequently, a number of species associated with the oyster and Sabellariacommunities disappeared too, and many new species, mainly polychaetes, invaded the area. At present, in terms of species richness, benthic communities in the northern Wadden Sea are dominated by polychaetes (REISE, 1982). In the subtidal western Wadden Sea essentially the same changes may have occurred. Oyster fisheries occurred in the Dutch Wadden Sea up until the first decade of this century. HOEK (1901) reported living O. edulis and fishery on this species at various subtidal localities in the western Dutch Wadden Sea, but it is considered extinct in the Dutch Wadden Sea at present. Sabellaria-reefs have never been recorded for this area. The number of species in the subtidal is quite high in comparison with that in the intertidal of the western Wadden Sea: 80 species in the subtidal and 41 in the intertidal (BEUKEMA, 1976). Approximately the same ratio was also found in the Oosterschelde, with 134 species in subtidal and 59 in intertidal areas (FORTUIN, 1981). This is probably a common feature. It might be explained by the extreme environment in the intertidal. The greater number of species in the Oosterschelde than in the Wadden Sea is probably related to the higher and more constant salinity, and the lower silt load of the water. A comparison of the species lists of the subtidal areas of the Oosterschelde (FORTUIN, 1981) and the western Wadden Sea finds 71 species in common. 11 out of 80 species (14%) have been found in the subtidal Dutch Wadden Sea only. 65 out of 134 species (49%) were only found in the subtidal Oosterschelde.

65

TABLE 6 Frequency of occurrence of some widespead macrobenthic invertebrates in the subtidal Oosterschelde (FORTUIN,1981) and subtidal western Dutch Wadden Sea (this study).

Oosterschelde

WaddenSea

39% 33% 25% 57% 30% 29% 43% 17%

82% 42% 50% 70°,/o 36% 35% 40% 55%

Macoma balthica Eteone Ionga Nephtys hombergii Scoloplos armiger Spio filicornis Magelona papillicornis Capitella capitata Heteromastus filiformis

Subtidal flats, a characteristic component of the western Dutch Wadden Sea, occupy only very limited areas in the Oosterschelde. Nevertheless, the common macrofauna shows a considerable similarity. In general, the subtidal soft-bottom community in the Oosterschelde estuary is richer in terms of species number, and probably shows more spatial variation, while in the western Wadden Sea the common species generally show more uniform distribution patterns (Table 6). Both numerical densities and biomass values of Hydrobia ulvae are high in the subtidal, which has not been reported before from subtidal areas in the Wadden Sea. In the intertidal Wadden Sea, however, locally high densities and biomass of Hydrobia may be present (ASMUS & ASMUS, 1985; BEUKEMA, 1988). For intertidal Hydrobia, microphytobenthos is considered to be the main food source, with detritus-bound bacteria as additional food source (JENSEN & SIEGISMUND, 1980). Due to high water turbidity, in the subtidal areas benthic primary production is expected to be low, so the main food source for subtidal Hydrobia remains unclear.

TABLE 7 Comparison of total macrozoobenthic biomass values (g.m -2 AFDW) in subtidal and intertidal parts of the Wadden Sea (W.S.), the share of Mytilus edulis included and excluded.

Area Subtidal W. Dutch W.S. (Texelstroom) E. Dutch W.S. (Zoutkamperlaag) Ems outer estuary W. Dutch W.S. Intertidal W. and E. Dutch W.S. (1971-72) W. Dutch W.S. (1971-72) W. Dutch W.S. (1977) W. Dutch W.S. (Balgzand 81-83) W. Dutch W.S. (1987) Ems outer and middle estuary W. German W.S. (Randzel) W. German W.S. (Jadebusen)

Biomass incl. Mytilus excl. Mytilus

Source

17 16.5 1.8 43.7

4 8.9 1.8 15.0

BEUKEMA, 1977 HAVERKAMP, 1981 VAN ARKEL& MULDER, 1979 This StUdy

26.6 20.1 19.3 52.3 38.5 8.1 109 52

20.4 19.2 16.3 45.6 37.6 8.1 36 43

BEUKEMA, 1976 BEUKEMAet al., 1978 BEUKEMAet al., 1978 Beukema, pers. comm. BEUKEMA, in press. VAN ARKEL & MULDER, 1979 OBERT, 1982 MICHAELIS, 1987

66

R. DEKKER

The high biomass of Mytilus edulis in the deeper areas of the western Dutch Wadden Sea is mainly due to the wild mussel beds, which were found several times, and are reported at depths down to 20-25 m (VERWEY, 1983). The high biomass value for Mytilus in the deepest parts of the subtidal (> 10 m) should be viewed with reserve. This value is based on one sample in a dense wild mussel bed, out of only 18 samples in the stratum >10 m, which resulted in a high standard error and consequently wide 95% confidence limits (Table 5). The total biomass of the subtidal area of the western Dutch Wadden Sea was higher than subtidal areas of nearby estuarine systems. In the outer Ems estuary, German-Dutch Wadden Sea, the macrozoobenthic biomass of the subtidal area, sampled with a Van Veen grab, amounted to 1.8 g,m -2 AFDW (VAN ARKEL & MULDER, 1979). During their survey in 1974/1975 no subtidal stocks of Mytilus edulis were found and mussel culture was not practised in this area of the Wadden Sea during that period. Even with the share of Mytilus excluded from the total biomass in the subtidal western Dutch Wadden Sea, its value would be 15 g.m -2 AFDW. A comparison of biomass data of subtidal macrobenthos in other parts of the Wadden Sea is given in Table 7. In a part of the Oosterschelde estuary COOSEN & VAN DEN DOOL (1983) found quite high subtidal macrofaunal biomass values at 18 subtidal stations. During spring sampling (April 1980) they found a biomass of 16.3 g.m -2, and during autumn (September 1980) a subtidal biomass of even 28.4 g.m -2, of which at least 85% was formed by Mytilus edulis. For an estimate of the relative importance of the subtidal macrofauna, a comparison might be made with the status of the intertidal macrofauna in the Wadden Sea. As Mytilus edulis shows very different biomass values in the different study areas because of the highly aggregated distribution and presence or absence of mussel culture, the biomass data of these areas are presented including and excluding the share of Mytilus (Table 7). Including the share of Mytilus the macrozoobenthic biomass of the subtidal western Dutch Wadden Sea is within the range of that of intertidal areas in the Wadden Sea. This is in contradiction with the general opinion, based on more fragmentary subtidal sampling, that subtidal macrozoobenthic biomass in the Dutch Wadden Sea is of minor importance compared with intertidal macrozoobenthos (BEUKEMA, 1977, 1983; VAN ARKEL & MULDER, 1979, but see HAVERKAMP, 1981). With Mytilus excluded from the biomass data, the values for the remaining macrozoobenthic biomass of the subtidal western Dutch Wadden Sea are low compared to the corresponding values observed for intertidal areas (Table 7). Reports on rich macroben-

thic assemblages in the subtidal German Wadden Sea, however, lack biomass data (RIESEN & REISE, 1982; REISE & SCHUBERT, 1987). Comparisons between the share of various species in the subtidal and the intertidal for the same region and period (Table 5) demonstrate the marked importance of Hydrobia ulvae, Mytilus edulis and Carcinus maenas in the subtidal, and the relative absence of Cerastoderma edule, Mya arenaria and Arenicola marina. The shares of the groups of filter feeders and deposit feeders are remarkably equal in the two areas. Only the share of the carnivorous invertebrates increases towards greater water depths. The subtidal was dominated by epibenthic, the intertidal by endobenthic macrozoobenthos. In the Dutch Wadden Sea, subtidal mussels beds occur also under natural conditions, both in the western part before mussel culture started in 1950 (VERWEY, 1983) and in the eastern part, where no mussel farming is executed (HAVERKAMP, 1981). Due to mussel farming the total densities of Mytilus edulis have increased, both by net transport of seed mussels from intertidal beds to subtidal culture plots and by reduction of predators by the mussel farmers. The biomass of Mytilus in the subtidal western Dutch Wadden Sea outside the mussel culture plots, viz. 10.3 g.m -2 AFDW (Table 4), was not very different from that on intertidal Balgzand and subtidal Zoutkamperlaag (Table 7), which were both about 7 g.m -2 AFDW. The surplus of Mytilus biomass, about 18 g-m-2 AFDW, should hence be considered the man-made addition of mussel biomass to the macrozoobenthic biomass in the western Dutch Wadden Sea. 6. REFERENCES

ARKEL, M.A. VAN & M. MULDER,1975. A device for quantitative sampling of benthic organisms in shallow water by means of a flushing technique.--Neth. J. Sea Res. 9: 365-370. ----, 1979. Inventarisatie van de macrobenthische fauna van het Eems-Dollard estuarium. BOEDE Publ. & Versl. 1979-2 (unpubl. report): 1-122. ARNTZ, W.E. & H. RUMOHR, 1986. Fluctuations of benthic macrofauna during succession and in an established community.-- Meeresforsch. 31:97-114. ASMUS, H. & R. ASMUS, 1985. The importance of grazing food chain for energy flow and production in three intertidal sand bottom communities of the northern Wadden Sea.--Helgol&nder Meeresunters. 39" 273-301. BEUKEMA,J.J., 1974a. The efficiency of the Van Veen grab compared with the Reineck box sampler.--J. Cons. int. Explor. Mer 35: 319-327. ----, 1974b. Seasonal changes in the biomass of the macrobenthos of a tidal flat area in the Dutch Wadden Sea.--Neth. J. Sea Res. 8:94-107

ZOOBENTHOS OF SUBTIDAL WADDEN SEA

, 1976. Biomass and species richness of the macrobenthic animals living on the tidal flats of the Dutch Wadden Sea.--Neth. J. Sea Res. 10: 236-261. , 1977. De rol van bodemdieren in de voedselketens van de zee.--Vakbl. Biol. 57" 284-287. , 1982. Annual variation in reproductive success and biomass of major macrozoobenthic species living in a tidal flat area of the Wadden Sea.--Neth. J. Sea Res. 16: 37-45. , 1983. Quantitative data on the benthos of the Wadden Sea proper. In: W.J. WOLFF. Ecology of the Wadden Sea, Vol. 1, Pt 4. Balkema, Rotterdam: 134-142. , 1988. An evaluation of the ABC-method (abundance/biomass comparison) as applied to macrozoobenthic communities living on tidal flats in the Dutch Wadden Sea.--Mar. Biol. 77: 425- 433. ,1989. Long-term changes in macrozoobenthic abundance on the tidal flats of the western Wadden Sea.--Helgol&nder Meeresunters. (in press). BEUKEMA, J.J. & G.C. CADI~E, 1986. Zoobenthos responses to eutrophication of the Dutch Wadden Sea.--Ophelia 26: 55-64. BEUKEMA, J.J. & K. ESSINK, 1986. Common patterns in the fluctuations of macrozoobenthic species living on different places on tidal flats in the Wadden Sea.-Hydrobiologia 142: 199-207. BEUKEMA, J.J., W. DE BRUIN & J.J.M. JANSEN, 1978. Biomass and species richness of the macrobenthic animals living on the tidal flats of the Dutch Wadden Sea: long-term changes during a period with mild winters.--Neth. J. Sea Res. 12: 58-77. BREY, T., 1986. Formalin and formaldehyde-depot chemicals: effects on dry weight and ash free dry weight of two marine bivalve species.--Meeresforsch. 31 : 52-57. COOSEN, J. & A. VAN DEN DOOL, 1983. Macrobenthos van het Kram mer-Keeten-Volkerak estuarium. Verspreiding der soorten, aantallen en biomassa in relatie met het zoutgehalte. Zachtsub eindrapport, DIHO-DDMI (unpubl. report): 1-131. DANKERS, N., 1986. Onderzoek naar de rol van de mosselkultuur in de Waddenzee. RIN Rapport 86/14 (unpubl. report): 1-36. DANKERS, N., H. KOHL & W.J. WOLFF, 1983. Invertebrates of the Wadden Sea. In: W.J. WOLFF. Ecology of the Wadden Sea, Vol. 1, Pt 4. Balkema, Rotterdam: 1-221. DEKKER, a., 1982. Vergelijking van de bruikbaarheid van de Van Veen-happer met de Van Arkel-flushing sampler voor het bemonsteren van het sublittorale macrobenthos van de Waddenzee. NIOZ Interne Versl. 1982-9 (unpubl. report): 1-9. DITTMER, J.-D., 1983. The distribution of the subtidal macrobenthos in the estuaries of the rivers Ems and Weser. In: W.J. WOLFF. Ecology of the Wadden Sea, Vol. 1, Pt 4. Balkema, Rotterdam: 188-206. ENTE, P.J., 1987. Bodemkundig onderzoek westelijke Waddenzee tussen GLW en N A P - 5 m . RIJP Rapport 1987-1CBW (unpubl. report): 1-89.

67

ESSINK, K., 1978. The effects of pollution by organic waste on macrofauna in the eastern Dutch Wadden Sea.-NIOZ Publ. Ser. 1" 1-135. FORTUIN, A.W., 1981. Samenstelling, verspreiding, aantallen en biomassa van het macrozoobenthos in het Volkerak-Oosterschelde estuarium in de periode 1959 tim 1976. DIHO Rapp. & Versl. 1981-6 (unpubl. report): 1-237. HAVERKAMP, S.J., 1981. Een onderzoek naar de gevolgen van de afsluiting van de Lauwerszee in 1968/1969 op de bodemfauna van de Zoutkamperlaag in 1980. RIZA rapport BI-MV 80.10 (unpubl. report): 1-43. HOEK, P.P.C., 1901. Schelpdierenteelt in het Noordelijk deel der Zuiderzee. In: Verslag van den Staat der Nederlandsche Zeevisscherijen over 1900: 72-91. JENSEN, K.T. & H.R. SIEGISMUND, 1980. The importance of diatoms and bacteria in the diet of Hydrobiaspecies.--Ophelia, Suppl. 1: 193-199. KUIPERS, B.R., P.A,W.J. DE WILDE & F. CREUTZBERG, 1981. Energy flow in a tidal flat ecosystem.--Mar. Ecol. Progr. Ser. 5" 215-221. MICHAELIS, H., 1987. Bestandsaufnahme des eulitoralen Makrobenthos im Jadebusen in Verbindung mit einer Luftbild-Analyse.-- Forschungsstelle KL~ste 38: 13-98. MULDER, M. & M.A. VAN ARKEL, 1980. An improved system for quantitative sampling of benthos in shallow water using the flushing technique.--Neth. J. Sea Res. 14: 119-122. OBERT, B., 1982. Bodenfauna der Watten und Str&nde um Borkum-EmsmL]ndung.--Forsch. Stelle Insel- und KQstenschutz 33: 139-162. REISE, K., 1982. Long-term changes in the macrobenthic invertebrate fauna of the Wadden Sea: are polychaetes about to take over?--Neth. J. Sea Res. 16: 29-36. REISE, K. & A. SCHUBERT, 1987. Macrobenthic turnover in the subtidal Wadden Sea: the Norderaue revisited after 60 years.--Helgol&nder Meeresunters. 41: 69-82. RIESEN, W. & K. REISE, 1982. Macrobenthos of the subtidal Waddensea: revisited after 55 years.--Helgol&nder Meeresunters. 35: 409-423. VERWEY, J., 1983. The blue mussel Mytilus edufis. In: W.J. WOLFF. Ecology of the Wadden Sea, Vol. 1, Pt 4. Balkema, Rotterdam: 114-115. WILDE, P.A.W.J. DE & J.J. BEUKEMA, 1984. The role of the zoobenthos in the consumption of organic matter in the Dutch Wadden Sea.--NIOZ Publ. Ser. 10: 145-158. WOLFF, W.J., 1973. The estuary as a habitat--Zool. Verhand. 126: 1-242. WOLFF, W.J. & N. DANKERS, 1983. Preliminary checklist of the zoobenthos and nekton species of the Wadden Sea. In: W.J. WOLFF. Ecology of the Wadden Sea, Vol. 1, Pt 4. Balkema, Rotterdam: 24-60. WOLFF, W.J. & L. DE WOLF, 1977. Biomass and production of zoobenthos in the Grevelingen estuary, the Netherlands.--Estuar. coast, mar. Sci. 5: 1-24. (received 8 July 1988; revised 6 December 1988)

68

R. DEKKER

APPENDIX List of all macrozoobenthic species found during the survey in the sublittoral western Dutch Wadden Sea. The species are divided into: filter feeders (F), deposit feeders (D), omnivores (O) and carnivores (C), and also into epifaunal (e), shallow endofaunal (s) and deep endofaunal (d) species. Species marked with * occurred in less than 1% of the samples. COELENTERATA Metridium senile (Linnaeus, 1761) Sagartia troglodytes (Price, 1847) Sagartiogeton undatus (Muller, 1788)*

Fe C s C e

NEMERTINA not specified

C s

MOLLUSCA

Hydrobia ulvae (Pennant, 1777) Retusa obtusa (Montagu, 1803) Onchidoris bilamellata (Linnaeus, 1767)* Aeolidia papillosa (Linnaeus, 1761)* Mytilus edulis Linnaeus, 1758 Mysella bidentata (Montagu, 1803)* Cerastoderma edule (Linnaeus, 1758) Petricola pholadiformis Lamarck, 1818 Spisula subtruncata (Da Costa, 1778)* Abra alba (Wood, 1802) Scrobicularia plana (Da Costa, 1778)* Macoma balthica (Linnaeus, 1758) Angulus fabula (Gmelin, 1791)* Angulus tenuis (Da Costa, 1778) Mya arenaria Linnaeus, 1758 OLIGOCHAETA not specified

D C C C F F F F F D D D D D F

e s e e e s s s s s s s s s d

Ds

POLYCHAETA Harmothoe imbricata (Linnaeus, 1767) Harmothoe impar (Johnston, 1839)* Harmothoe lunulata (Delle Chiaje, 1841) Harmothoe sarsi (Kinberg, 1865)* Pholoe minuta (Fabricius, 1780)* Eteone Ionga (Fabricius, 1780) Eteone picta Quatrefages, 1865" Anaitides maculata/mucosa Eulalia viridis (Linnaeus, 1767)* Microphthalmus similis Bobretzky, 1870" Nereis diversicolor O.F. M~ller, 1776

Ce Ce 0 s 0 s Cs Cs Cs Cs 0 e 0 s 0 s

Nereis succinea Frey & Leuckart, 1847 Nereis virens M. Sars, 1835 Nereis Iongissima Johnston, 1840 Nephtys cirrosa Ehlers, 1868 Nephtys hombergfi Savigny, 1818 Nephtys caeca (Fabricius, 1780) Nephtys Iongosetosa Oersted, 1843 Scoloplos armiger (O.F. MLiller, 1776)

Os Os Ds Cs Cs Cs Cs Ds

Aricidea minuta Southward 1956 Paraonis fulgens (Levinsen, 1883) Spio filicornis (O.F. MOiler, 1766) Polydora ligni Webster, 1879" Polydora ciliata (Johnston, 1838) Pygospio elegans Claparede, 1863 Spiophanes bombyx Claparede, 1870 Scolelepis foliosa (Audouin & Milne-Edwards, 1834) Scolelepis squamata (O.F. ML~ller, 1789)* Scolelepis bonnieri (Mesnil, 1896) Streblospio shrubsolii (Buchanan, 1890) Magelona papillicornis F. ML~ller, 1858 Tharyx marioni (Saint-Joseph, 1894) Travisia forbesfi Johnston, 1840 Capitella capitata (Fabricius, 1780) Heteromastus filiformis (Claparede, 1864) Arenicola marina (Linnaeus, 1758) Pectinaria koreni Malmgren, 1865 Lanice conchilega (Pallas, 1766) CRUSTACAEA Balanus spec. (not quantified) Gastrosaccus spinifer (Goes, 1864) Gastrosaccus sanctus (Van Beneden, 1861)* Schistomysis kervillei (G.O. Sars, 1885)* Neomysis integer (Leach, 1814)* Diastylis bradyi Norman, 1879" Lamprops fasciata G.O. Sars, 1863 Gammarus Iocusta (Linnaeus, 1758) Gammarus duebeni Liljeborg, 1852 Chaetogammarus marinus (Leach, 1815)* Bathyporeia elegans Watkin, 1938" Bathyporeia guilliamsoniana (Bate, 1856)* Bathyporeia pelagica (Bate, 1856) Bathyporeia pilosa LindstrSm, 1855" Bathyporeia sarsi Watkin, 1938 Urothoe poseidonis Reibisch, 1905 Urothoe elegans (Bate, 1856)* Pontocrates altamarinus (Bate & Westwood, 1862)* Corophium arenarium Crawford, 1937 Crangon crangon (Linnaeus, 1758) Carcinus maenas (Linnaeus, 1758) ECHINODERMATA Asterias rubens Linnaeus, 1758 Ophiura texturata Lamarck, 1816" Echinocardium cordatum (Pennant, 1777)*

D D D D D D D

s s s s s s s

O D D D D D D D D D D D

s s s s s s s s d d s s

F e De D e D e D e Ds Ds De De D e Ds D s Ds Ds D s D s D s D D C C

s s e e

C e Ce Ds