Benthic marine fauna structured by hydrodynamic processes and food availability

303

Netherlands Journal of Sea Research 34 (4): 303-317 (1995)

BENTHIC MARINE FAUNA STRUCTURED BY HYDRODYNAMIC PROCESSES AND FOOD AVAILABILITY RUTGER ROSENBERG GStebo~ U n i v e ~ Kris~ebe~ Ma~eResearchS~n, 4 ~ ~ Fiskeb~skiI, Sw~en

ABSTRACT Benthic macrofauna was investigated, mainly in clayey silt sediments, on the west and east slopes (65-90 m depth) and at the bottom (~100 m depth) of a trench in the Skagerrak, western Sweden. The western slope is an underwater delta front area with, at least intermittently, strong bottom currents transporting suspended organic and inorganic particles. In the deeper parts, currents slow down and accumulation is extremely high (mean ~J0 mm.y"). The benthic community on the wsstem slope was dominated by the passive suspension-feeding brittle star Amphiura filiformis. Its numbers and biomass were much larger than recorded in the Skagerrak and the North Sea. Total community abundance and number of species were significantly larger on the western slope than on the eastern. In the deep part of the trench significantly higher abundance and number of species were recorded than on the slopes. Dominant in the deep were the small polychaetes, Heteromastus filiformis and ParamphinomeJeffreysi, both assumed to be sub-surface deposit feeders. Faunal distribution and richness are discussed in relation to food availability through advective near-bottom processes on the western slope, and in relation to accumulation at the bottom of the trench. The extreme densities and biomasses recorded on the western slope suggest that these communitiss were limited by space rather than by food. In contrast, similar communities characterized by A. •iformis in the Skagerrak and the North Sea have significantly lower abundance and biomass, and are therefore thought to be food limited.

Key words: Sediment structure, particle transport, accumulation, feeding mode, food limitation, Skagerrak, Amphiura filiformis, A. chiajei, Mysella bidentata, Heteromastus filiformis, Paramphinome jeffreysi

1. INTRODUCTION The role of biotic and abiotic factors in structuring marine benthic communities has been a focus for ecological research for several decades. Since the days of Petersen's (Petersen, 1913) pioneering work on benthic communities, scientists have agreed that the distribution of animal communities is largely influenced by physical factors. The importance of sedimentary characteristics for the geographical distribution of benthic assemblages was developed and summarized by Jones (1950). Other studies have shown that distribution of suspension-feeding animals on soft-bottom sediments was largely restricted to sandy habitats (Gray, 1974). Rhoads & Young (1970) suggested that trophic group amensalism was a reason for this, Le. that the reworking activity of deposit feeders disturbed or prevented the establishment of suspension feeders in silt-clay bottom sediments. The

effects of biological interaction on the structure of shallow water communities has also been demonstrated by e.g. Woodin (1983), who classified benthic populations into functional groups. In two review papers Pearson & Rosenberg (1978, 1987) suggested that benthic animals in general may be organized structurally, numerically, and by feeding mode in relation to food availability and to organic enrichment of surface sediments. A direct coupling between the food produced in the pelagic system and consumed in the benthic system can be demonstrated (Hargrave, 1973). The concentration of organic matter in the water column generally attenuates with depth. In areas where water front systems occur, favourable conditions for localized high plant production may occur and lead to high sedimentation of organic matter, supporting a locally enhanced benthic biomass. An example of this type of benthic-pelagic coupling is found in a tidal front area at

304

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Fig. 1. The Deep Trench in the southeastern Skagerrak with depth contours (A). The area inside the rectangle is enlarged in Fig, 1B and shows the approximate position of the sampling areas/stations for fauna and sediment (P- and D-stations) and depth contours. At stations with filled circles suspended organic material was sampled. Fig, 1C (modified after Rodhe 1973) shows the profile of the bed rock with overlying sediment profile of the bottom with the D-stations indicated: Below is the approximate annual accumulation given in mm.

STRUCTURING FACTORS FOR BENTHIC FAUNA

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May 1992 four samples were taken at each of the areas/stations D1-D5. Samples at st. D1 and D5 were randomized at depths between 65 and 70 m, and st. D2 and D4 at depths between 85 and 90 m. St. D1 and D2 were on the east side of the Deep Trench and st. D4 and D5 on the west side. Samples at st. D3 were taken at random in the deepest (-100 m) area. In October 1992 samples from another three stations, P1, P2 and P3, were randomized and taken in a similar way from the deepest part of the Deep Trench north of the D-stations. The sediment was sieved on l-ram mesh, preserved in 70% ethanol, and animals were later sorted out at 6 times magnification. Biomass is ethanol wet weight including mollusc shells. Four samples of the top 0 to 2.5 cm sediment were also taken from each station and analysed for particle size distribution (Department of Geology, GSteborg University), and content of organic C and total N analysed by a Carlo Erba (model 1106) elemental analyser after the sediment had been treated with acid to remove carbonaceous carbon. These results are expressed as percentages of sediment dry weight. Concentrations of suspended particles were analysed in 2-dm 3 water samples taken by a bottom released water sampler about 0.2 to 0.3 m above the bottom in the same depth intervals as the D-stations, but south of those positions (Fig. 1B). The water was filtered through 1 p.m pre-combusted GFF filters and ash-free dry weight (AFDW) was measured after burning at 500°C for 4 h. Sediment surface and bottom profile cameras were used to characterize the bottom. The sediment camera system is described in Rosenberg & Diaz (1993). The surface image covers ~1 m'; sediment profile images cover a 14.4 cm-wide vertical slice of the bottom sediment, and the height of these pictures is dependent on how deep the prism penetrates into the sediment. The cameras were deployed four to five times at each station and at each deployment one surface picture was taken and three sediment profile pictures at 2-second intervals. An Agfa CT 100 slide film was used and the images were transferred to CD and computer analysed in Adobe Photoshop to intensify contrasts in the sediment. At st. D4-D5 and P1-P3 the flash in the profile camera was not working properly and those images could only be partly analysed. Faunal means were tested for homogeneity (Cochran's test) and compared by ANOVA test followed by Contrast analysis using SuperANOVA (Abacus Concepts, 1989). Untransformed data were used, 2. MATERIAL AND METHODS except for Mysella bidentata where data were log-transformed. Numerical classification was used to Samples of benthic macrofauna were taken along two evaluate community differences by applying the transects (D and P, Fig. 1B), with a 0.1 m2 Bray-Curtis similarity coefficient to abundance data Smith-Mclntyre grab penetrating 18 cm into the bot- including all species, based on the group-average tom and filled at all hauls. The samples were rand- sorting algorithm (Bray & Curtis, 1957). Different mulomized at each station in relation to depth within a tivariate analyses produce generally similar results one-nautical-mile-wide area along the transect. In (Gray et aL, 1988). The animals were separated into

the Oyster Grounds in the North Sea (Creutzberg et aL, 1984). The horizontal flux of seston is also of great importance in transporting food near the bottom, which is obvious from extremely high secondary production measurements in suspension-feeding bivalves in shallow water (MSIler & Rosenberg, 1983). Secondary production can, in shallow water, be related to seasonal food supply and quality, which will have a short-term impact on deposit feeders (Cheng et aL, 1993; Marsh & Tenore, 1990). In mussel beds, turbulent mixing caused by the mussels creates strong vertical and horizontal gradients in fluorescence, which also influences the food availability to the benthic animals (Butman et aL, 1994). Physical energy above the sea bed is an important factor for the spatial distribution of different sediment types. In high energy areas, bottoms are commonly eroded and have a coarse sediment. Where bottom currents occur intermittently, episodic resuspension may take place, and in bottom areas with low energy, accumulation is likely to prevail. Advective processes also transport organic particles along the bottom, which may have an important impact on species composition and the feeding behaviour of benthic fauna, as is shown in this paper. Parallel to the Swedish west coast in the Skagerrak is an about 100-m-deep trench (the 'Deep Trench', Fig. 1) with connections to the deeper Norwegian Trench. West of the Deep Trench near-bottom advective water transport is at times high towards the centre of the Deep Trench and associated with transport of the highest concentrations of particles found in the Skagerrak (Van Weering et aL, 1993). Accumulation is extremely high (mean 90 mm-y") inthe deep part of the Deep Trench, but low (-1 mm.y") on the western and eastern slopes at some distance from the deep bottom (Rodhe, 1973; Fig. 1C). The hypothesis in this study is that the benthic faunal communities are structured by hydrodynamic processes and food availability. This will be evaluated by the following: (1) the benthic fauna on the western slope, with high transport rates of particles close to the bottom, differs from that on the eastern slope with low rates, and (2) the benthic fauna in the deepest part of the Deep Trench, with high accumulation rates, differs from that on the slopes. Parameters examined are benthic macrofaunal community structure, including the numbers of species and individuals, biomass, feeding types and sediment characteristics.

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TABLE 1 Benthic stations studied in the Deep Trench with positions,depths, suspended organic material (SOM) in bottom water, mean percent clay (<2 I~m)and silt (2-62 pro), mean percent C (S.E_<0.1) and N (S.E.<_0.01) and C/N in the top sediment. From sediment profile imagesthe following was estimated: mean number of biogenic voids in sediment, mean number of burrows, number of polychaetetubes at surface, and mean maximum sediment depth of animal activity (void, animal in burrow) in cm; numbers are estimated as means of 3-5 pictures per station. No data is indicated by -. Stations for sampling SOM were not identical with D-stations (see Fig. 1). stations position depth SOM sedim, structure sediment no. of depth of (m) mgAFDW clay silt C% N% C/N voids burrows tubes activity •dm-3 (%) (%) (cm) D1, eastslope D2, eastslope D4, west slope D5, westslope D3, deeptrench Pl, deep trench P2, deeptrench P3, deeptrench

57"55'37-11"18'71 67-70 57°55'20-11°17'35 85-89 57°54'74-11°14'36 85-90 57°54'25-11°11'70 69-70 57°54'85-11°15'02 99 57°57'50-11°12'40 104 57°56' 8-11°13'2 100 57°55' 9-11°13'9 100

0.2 0.5 6.5 1.9 21.5

19 22 21 18 26

feeding categories according to Fauchald & Jumars (1979) and Josefson (1986 & pers. comm.), except for Paramphinome jeffreysi, which was treated as a sub-surface feeder (see below), and Amphiura filiformis, which was treated as a suspension feeder (Buchanan, 1964). In recently conducted experiments A. filiformis started suspension feeding in currents above approximately 0.5 cm's -1 (L.O. Loo, pers. comm.).

28 60 70 71 65

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0.12 17.5 0.18 16.7 0.21 15.2 0.18 t5.6 0.2 16.0 0.24 14.2 0.22 14.1 0.24 13.7

1 1 1 I 1 ! 1 0.3

1 4

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5

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(1993) also described the Deep Trench as an area with peak accumulation rates with silty mud or mud, and stated that very low transmission levels indicative of suspended particles occur just west of the trench. The area west of this, the 'Skagen Flak', was characterized as an accumulation area where material from the North Sea, transported bythe Jutland Current, is deposited at rates of >2 mm-y-'. 4. RESULTS

3. DESCRIPTION OF THE DEEP TRENCH This first section is summarized from Rodhe (1973). During the last Quaternary glaciation the ice removed material down to about bed-rock in the study area (Fig. 1). With the retreat of the ice, about t3000 years ago, a rapid deposition of sediment occurred. The deposition is of delta-type; the material derived from the west and northwest where material is eroding from the bottoms. The western slope of the Deep Trench constitutes the delta front. Near-bottom currents (at times 50 cm's -1) to the west are strong enough to suspend and transport material towards the Deep Trench. With increasing depth, currents slow down and eroded material is deposited (Fig. 1C). Concentrations of suspended particles are variable, but measurements at several stations gave concentrations of 10 to 16 mg.dm 3 dry weight above the bottom. The accumulation rates west and east of the slopes are ~1 mm.y1, and at the bottom of the trench on average 90 mm.y-t, but with a maximum of 120 mm.y-1 (Fig. 1C). The sediment is characterized as green-grey silty clayey mud on the western slope and as grey-black silty clayey mud in the deeper parts. Temperatures of the bottom water vary between 5.0 and 8.0°C and salinity is close to 35 psu. The oxygen concentrations in the bottom water in May and October 1992 were >5.2 cm-3-dm-3 at all stations (own measurements). Denneg&rd et al. (1992) and Van Weering et al.

4.1. SEDIMENT CHARACTERISTICS AND CAMERA IMAGE OBSERVATIONS Positions, depths and sediment characteristics from the present investigation are given in Table 1. Amount of suspended organic material (SOM) in the bottom water was estimated on one occasion to evaluate whether parts of the suspended particles could be of organic origin. The highest values were recorded on the western slope and on the deep bottom of the Deep Trench. The top sediment was clayey silt with a little sand at st. D2 to D5, whereas sand dominated at st. D1. Percentages of C and N in the top sediment were lowest at station D1. A comparison between the eastern slope (st. D1 & D2) and the western slope (st. D4 & D5) gave significantly (13<0.001) higher percentages of C and N at the latter, whereas C/N ratios were significantly (p<0.001) higher at the eastern slope. Sediment surface and profile images from all stations showed that the sediment surface was rather smooth with many signs of animal activity, such as faecal pellets, polychaete tubes, furrows and burrows (Fig. 2, Table 1). The redox potential discontinuity appeared mainly to be close (<5 mm) to the sediment surface, but animal burrows, feeding voids and bioturbation showed that all sediments had many local areas where oxygen penetrated to a depth of several centimetres, The upper 2 to 4 cm of the sediment

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(D3, P1, P2, P3; depth range: 99-104 m) and the stations on the slopes (D1, D2, D4, D5; depth range: 67-90 m) demonstrated significantly larger numbers of species and individuals at the deeper stations, whereas no difference was found for biomass. The abundances at the P-stations were highest: between 1193 and 1364 ind.0.1 m "2. Benthic faunal similarity between stations clustered the deep stations (D3, P1, P2 and P3) into one group and the slope stations into another (Fig. 3). Among the deep stations, P-stations were grouped tightly together at higher similarity levels than st. D3. In the grouping among the slope stations, st. D1 had the lowest similarity with the others. To assess the comparative faunal dominance, the six numerically most abundant species/genera at each of the stations are listed in Table 3 and comprise in total 13 species/genera. The brittle star Amphiura filiformis was among the top two dominants at all the slope stations with numbers of >2500"m "2 at st. D2, D4 and D5. Their densities were significantly (p<0.001) higher at the western slope stations than at the eastern, and also at the four slope stations compared to at the four deep stations. Similar significant (p<0.05) differences were also calculated for A. chiajei. The small bivalve Mysella bidentata was among the three top dominants at st. D2-D5, with a maximum of 3335 ind.m "2. Significantly (p<0.001) larger 4.2. FAUNAL CHARACTERISTICS numbers were recorded at the western slope than at the eastern. Mean numbers of species, abundance and biomass At st. D3 the polychaete Heteromastus filiformis per sample (0.1 m 2) at the eight stations are given in reached the highest abundance of all and was also Table 2. Comparing the west side (st. D4, D5) with among the two top dominants at st. P1-P3. At all the eastern side of the slope of the Deep Trench (st. these four deep stations the abundance was D1, D2) showed that both the numbers of species >3000-m -2 and significantly (1:~-'0.001) higher than at and individuals were significantly larger on the west- the slope stations. The highest population record was ern side, whereas no difference was obtained for bio- for another p olychaete, Paramphinome jeffreysi, with mass (Table 2), because of high between-sample 7595 ind.m -2 at st. P2. While this species reached variation. A comparison between the deeper stations large numbers at the P-stations, it was almost absent at the D-stations. M. bidentata ranked number three at all P-stations and occurred in significantly TABLE 2 Mean number of species, abundance and biomass (g wet wt) (p<0.001) larger numbers at the deep stations than at per 0.1 m2 (and standard deviation) at stations in the Deep the slope stations. Species common at all stations Trench. p-values from contrast analysis between west side of were the polychaetes Pholoe minuta and Diplocirrus slope (D4, D5) and east side of slope (D1, D2), and between glaucus, and the bivalves Abra nitida and Nuculoma deepest stations (D3, P1, P2, P3) and slope stations (D1, D2, tenuis. D4, D5) are given at the bottom. The six dominants by weight are listed in Table 4 station species abundance biomass and comprise 17 species. The echinoderms BrissopD1 23.2 (2.2) 140 (35) 38 (23) sis lyrifera, A. filiformis and A. chiajei were the three D2 26.5 (3.9) 375(93) 71 (11) top dominants at six of the eight stations. The polychaetes H. filiformis, Polyphysia crassa, Hauchiella D4 32.5 (3.0) 780 (299) 54 (31) tribullata and P.jeffreysi generally had rather high bioD5 35.2 (5.1) 822 (152) 48 (6) masses at the deep stations (D3, P1, P2, P3), D3 26.5 (4.6) 705 (122) 60 (22) whereas another polychaete, Aphrodite aculeata, was P1 44.7 (2.5) 1361 (304) 21 (10) among the dominants at the two shallowest stations P2 30.5 (6.4) 1364 (128) 35 (35) (D1, D5). P3 40.2 (2.7) 1193 (275) 55 (20) Classification of the species into feeding categories D4/D5 - DI/D2 < 0.001 < 0.001 0.725 showed that suspension feeders were numerically Deep - Slope < 0.001 < 0.001 0.294 dominant at st. D2, D4 and D5 with 68 to 74% (Table

seemed generally to be well bioturbated and have a looser structure than deeper sediments. Black patches indicative of reduced conditions (Rhoads & Germano, 1986) and possibly organic enrichment were seen close to the surface at st. D2 and D3. Penetration of the profile camera into the sediment was between 8 and 13 cm. Activity of animals, recognized as burrows or active feeding voids, was found down to between 6 and 12 cm depth, but may also have occurred below the maximum penetration depth. Elongated, 2 to 4 cm-long red polychaetes, probably Heteromastus filiformis, were seen in many pictures (Fig. 2. 1), sometimes at depths down to 10 cm. An animal that appears to be Amphiura filiformis is seen with the disc at 3 to 4 cm below sediment surface and with structures for two arms connecting the disc to the sediment surface (Fig. 2.4). Objects that appeared to be arms of A. filiformis in the water could be seen at st. D2 and D3. Most feeding voids were observed at st. D2 and D3, and most polychaete tubes at the sediment surface at st. D3. In the surface images Ophiura spp. were observed at st. D4, D5, P1, P2 and P3 with maximum numbers of 8 ind. in one image at st. PI. At st. D3 one Pennatula phosphorea was seen and at st. P1 possibly one Finiculina quadrangularis, both of the Class Pennatulacea.

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Fig. 2. Sediment profile images from stations D1, D2 and D3 in the Deep Trench. The vertical scales are in centimetres. D1 (picture 1) shows loose material on the surface and a worm (probably Heteromastus filiformis) at 3 to 6 cm depth. D1 (picture 2) shows an active (oxidized) feeding void at 5 to 6 cm depth and patches of black sediment. D2 (picture 3) shows

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patches of black sediment, one worm (possibly H. filiformis) at 0 to 3 cm depth and one object at the surface that appears to be an arm of Amphiura filiformis. D3 (picture 4) shows tubes at the surface, several worms at 5 to 8 cm depth and apparently one A. filiformis with the disc at 3 to 4 cm depth and an arm connected with the surface.

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D1 D2 D4 D5 D3 P1 P3 P2 Fig. 3. Dendrogram showing the similarity between the benthic communities at the stations in the Deep Trench (Bray-Curtis similarity coefficient). 3). At stations on the bottom of the Deep Trench sub-surface feeders were the most common. The percent of predators was 11 or less. A similar separation into feeding groups was obtained by a classification based on biomass, with the exception of st. D2, where the proportion of sub-surface deposit feeders was slightly higher than that based on abundance. 5. DISCUSSION Both the slopes and the deep bottom of the Deep Trench accommodated a species-rich fauna with extremely high abundances and biomasses, and with biogenic activity occurring at depth in the sediment. On the slopes the highest numbers were found on the western side, where the suspension feeding Amphiura filiformis and Mysella bidentata were conspicuous dominants. On the eastern slope the fauna was tess rich, especially at st. D1, which had a sandier substrate. The lowered transport of particles accompanying lower food supply to that station is indicated by lower organic C and total N content of the sediment. The extreme biomass of A. filiformis on the western slope is most probably caused by transport of organic material along the bottom. This is indicated by the periodically strong current (Rodhe, 1973), and several measurements demonstrate that the near-bottom water has high particle concentrations (Rodhe, 1973; Van Weering etaL, 1993), which also seems to contain high concentrations of suspended organic material. Thus, it is suggested that this downward directed advection along the bottom

slopes favours suspension-feeding macrofauna. A. filiformis and M. bidentata are known to live in association with each other and their numbers have been shown to be correlated in some areas (Ockelmann & Muus, 1978). This was not the case in this study, possibly because M. bidentata was able to obtain food on both the transport and the accumulation bottoms. It has been shown that M. bidentata, in addition to suspension feeding, can also inhale sediment particles re-suspended by themselves (Ockelmann & Muus, 1978). The ability of this species also to use deposited particles may explain their high abundance in areas where high accumulation occurred. On the bottom of the Deep Trench, at only a small distance from the slope stations and only slightly deeper, the polychaetes Heteromastus filiformis and Paramphinome jeffreysi were the numerical dominants, and Mysella bidentata also occurred in large numbers. Faunal composition here differed clearly from that on the slopes as shown by the numerical classification analysis. St. D3 was sampled in spring and st. P1-P3 in autumn the same year, but the seasonal variation at this depth in the Skagerrak is insignificant (Josefson, 1981). The difference between the slopes and the deep part of the trench is therefore probably due to spatial rather than temporal differences. H. filiformis is a sub-surface deposit feeder. The feeding mode of R jeffreysi is not clear, but it is here also classified as a sub-surface deposit feeder (see below). A high accumulation rate was indicated by high percentages of C and N in the sediment. Lower C/N ratios at the P-stations than at the D-sta-

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TABLE 3 Abundance per m2 of the six dominant species at each station. Total abundance at station and percentagenumbers belonging to different feeding groups are also given. species slope stations deep stations D1 D2 D4 D5 D3 P1 P2 P3 Amphiura fififormis 283 2 5 2 0 3 6 3 8 2563 1343 270 378 785 Abra nitida 223 168 90 280 265 140 105 133 Amphiura chiajei 208 83 150 268 123 63 78 218 Philomedes globosus 170 8 0 0 0 0 0 0 Mysella bidentata 115 273 1 6 3 0 3335 1448 2480 1138 2178 Diplocirrus glaucus 38 53 83 108 43 120 63 108 Heteromastus fififormis 30 130 300 40 3025 3660 3323 4213 Nuculoma tenuis 15 70 310 100 73 178 138 173 Pholoe minuta 5 63 410 500 168 380 208 518 Lapidoplax buskii 0 0 335 75 18 0 0 0 Onoba sp. 3 10 70 270 0 0 5 13 Paramphinome jeffreysi 0 0 3 0 0 4810 7595 2515 Hauchiella tribullata 0 0 0 0 28 665 223 303 Total abundance at station Suspension feeders (%) Surface deposit feeders (%) Sub-surface depost feeders (%) Predators (%)

1398 31 51 7 11

3753 74 12 7 7

tions suggest that the upper sediments at the former had the highest nutritious value. A similar difference may exist between the western slope, with lower C/N ratios, and the eastern slope. Although the upper centimetres of the sediment were reworked, the RPD was close to the sediment surface at all stations, suggesting a high oxygen demand of the top sediment. This may be a result of a large supply of organic material to the bottoms. One of the dominants in the deep sediments of the Deep Trench, Heteromastus filiformis, has a wide distribution in the Skagerrak with highest and rather stable densities of 1000-2000 ind.m "2 at about 100 m depth (Josefson, 1981, 1985). The densities were higher in the present investigation, but numbers of >5000 ind.m -2 have been recorded in the intertidal (Shaffer, 1983). The abundance of H. filiformis in the Deep Trench may have been underestimated as the grab only penetrated down to maximally 18 cm into the sediment. H. filiformis is a head-down sub-surface deposit feeder ingesting sediment from as deep as 15 to 20 cm below the sediment surface (Josefson, 1981; Clough & Lopez, 1993). H. filiformis burrows into the sulphidic environment in the sediment; it feeds selectively, and transports large amount of pelletized material to the sediment surface (Neira & H~pner, 1994). Its distribution has in several studies been associated with organic enrichment (Pearson & Rosenberg, 1978). Another polychaete, Paramphinome jeffreysL also appeared in very high densities at the deep sites. At

7798 68 13 10 9

8223

7055

72 12 6 10

40 10 45 6

13615 20 10 64 5

13643 11 4 82 3

11928 25 9 59 7

Josefson's (1986) 100-m station, north of the study area, he found densities of between ~50 and -1000 ind-m -2 from 1970 to 1982. This species has been recorded 10 cm below the sediment surface (Josefson, 1981; Romero-Wetzel & Gerlach, 1991). The feeding mode of R jeffreysi is not known. Amphinomids are frequently found associated with corals and beach-rocks and are then suggested to be carnivores (Fauchald & Jumars, 1979). Their high densities and position buried rather deep in the sediment may indicate that they are able to behave as sub-surface deposit feeders, but this has yet to be established. The other abundant polychaetes, Hauchiella tribullata and Pholoe minuta, are deposit feeders and predators, respectively. Thus, sub-surface deposit feeders greatly predominate on the sediment-accumulation bottoms; their dominance is substantial since P. jeffreysi was also classified in that feeding group. Josefson (1985) also concluded from his studies in the Skagerrak that sub-surface deposit feeders have highest densities on the lower shelf where accumulation of organic matter is highest. The lower proportion of surface deposit feeders than of sub-surface deposit feeders may be due to the fact that surface feeders commonly rely on newly deposited organic matter, which is not present at these depths, or that predation at the surface favours animals living and feeding deeper in the sediment. Also the sediment images clearly showed activity down to depths where these polychaetes have been reported in other studies. It has been pointed

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TABLE 4 Biomass (g wet weight per m2) of the six dominant species at each station. Total biomass at station, and percentage biomass belonging to different feeding groups are also given.

species Brissopsislyrifera Amphiura filiformis Amphiura chiajei Chaetopterus variopedatus Aphrodita aculeata Abra nitida Echinocardium cordatum Calocaris macandreae Heteromastus filiformis Polyphysia crassa Pachycerianthus multiplicatus Anobothrus gracilis Nuculoma tenuis Mysella bidentata Abra alba Hauchiella tribullata Paramphinomejeffreysi

D1 144.1 75.8 62.8 36.2 26.4 7.9 0.0 0.2 0.1 0.0 0.0 0.3 0.1 0.3 0.0 0.0 0.0

slope stations D2 D4 279.6 95.7 341.8 451.1 23.7 46.6 0.0 0.0 0.0 0.0 3.8 2.1 21.2 8.8 4.0 0.0 0.6 0.8 0.0 0.0 0.0 0.0 1.5 4.7 0.7 4.1 0.7 4.1 0.0 0.0 0.0 0.0 0.0 0.0

D5 0.0 306.3 108.2 1.8 22.6 11.2 0.0 0.0 0.5 0.0 0.0 1.0 0.5 8.9 5.3 0.0 0.0

D3 217.6 273.9 47.t 0.0 0.0 3.0 0.0 0.0 16.8 149 46 ~.2 06 40 0.0 3.! 0.0

Total biomass at station

378.2

721.0

481.8

595.2

65 27 1 7

47 9 42 1

Suspension feeders (%) Surface deposit feeders (%) Sub-surface deposit feeders (%) Predators (%)

32 19 39 11

50 7 41 2

out in several papers (Lopez & Levinton, 1987) that deposit feeders subsist on a remarkably poor food source, but usually at low or moderate densities. In shallow waters, however, deposit feeders can respond to seasonal food input to the sediment (Cheng et aL, 1993). The high accumulation of organic material in the deepest part of the Deep Trench seems to allow this site to accommodate a rich fauna of deposit-feeding animals. The communities in the Deep Trench can tolerate high sedimentation rates in the order of 90 mm-y "1. In a study of the East China Sea in a rapidly sedimenting (20 to 50 mm.y -1) submarine delta, sparse populations of small polychaetes were found to dominate (Rhoads et al., 1985). There are few other studies in which sub-tidal benthic faunal composition and quantity have been related to marine physical processes and food availability. At a tidal front area on the Oyster Grounds in the North Sea, several Dutch researchers have studied similar phenomena. Here, a dramatic drop of current speed over a short distance created favourable conditions for particles to settle, just as in the Deep Trench. Over a distance of about 10 nautical miles on the Oyster Grounds, both the faunal and sediment structures changed significantly. In the silt-clay sediment with the highest sedimentation of fresh organic

632.2 73 10 16 1

deep stations P1 P2 61.1 1 6 9 . 7 7.2 35.7 9.1 36.6 0.0 0.0 12.2 0.0 2.4 4.9 0.1 0.0 0.0 0.0 19.2 16.7 8.0 34.3 13.6 0.0 0.8 0. t 1.3 2.8 3.5 2.2 0.0 0.0 42.8 10.3 11.3 18.2 207.5 6 30 53 12

355.4 11 15 69 5

P3 178.4 105.9 87.7 0.0 0.0 4.6 10.5 0.0 24.8 72.3 7.9 0.5 2.4 4.2 0.0 29.6 7.7 552.6 20 25 54 1

material (Cramer, 1990), Amphiura filiformis was the dominant species. Other dominants here were the suspension feeders Turritella communis and Chaetopterus variopedatus (Creutzberg et aL, 1984). The authors also showed that deposit feeders dominated in the muddy sand area in front of the region of high sedimentation. In the Kiel Bay in the southwest Baltic the importance of the spring phytoplankton bloom as food for the benthic system was assessed. At a 21-m-deep station with sandy mud, dominated by the sub-surface deposit feeding potychaete Pectinaria korenL the carbon demand by that community was not supplied by enough food from the sedimentation subsequent to that spring bloom (Graf et al., 1982). The authors suggested that a near-bottom transport of organic particles may had supplied the benthic fauna with additional food. In a study from the North Sea, Duineveld et al. (1987) showed that A. filiformis is positively correlated with the percentage of mud content. Thus, as also shown in the Deep Trench, passive suspension feeders may dominate on silt-clay bottoms when current speed is favourable and food available. This contradicts the common finding that suspension feeders mainly occur on predominantly sandy bottoms (summarized in the review by Gray, 1974). The sediment

STRUCTURING FACTORS FOR BENTHIC FAUNA on the slopes (st. D2, D4, D5) consisted predominantly of silt-clay. The same granular sizes dominated at the deep station D3, and seem to prevail throughout the accumulation area (Denneg&rd et aL, 1992), including the P-stations. Thus, the sediment structure on both slopes (excluding st. D1) and on the bottom of the Deep Trench was almost the same and the percentages of C and N were similar. The main difference between these two habitats is, therefore, suggested to be that the slopes are areas where downward directed advection of particles normally prevails, and the deep bottoms are areas where accumulation prevails. This difference seems to be the major structuring factor for the benthic communities and not sediment structure per se. In the southwest Baltic, benthic fauna was investigated in several small channel areas down to about 30 m depth (Arntz et aL, 1976). The highest number of species, abundance and biomass were found on the slopes (15-25 m). The fauna was dominated by molluscs and the authors attributed the favourable conditions on the slopes to relatively stable temperatures, increased salinity in these stratified brackish waters, sediment characteristics (50% silt-clay), and a heavy 'rain' of larvae and detritus. The deep parts of these channels are periodically poor in oxygen. It seems likely that these rich zones on the slopes, as in the Deep Trench, were influenced by transport of organic material along the bottoms. The importance of horizontal seston flux for growth rates in bivalves has been assessed by, e.g. Grizzle & Morin (1989). Recently it was shown that turbulent mixing were several times higher over a mussel bed (Mytilus edulis) than over a smooth bottom (Butman et aL, 1994). It is possible that dense mats of A. filiformis arms also create enough turbulent mixing just above the bottom to increase the food availability. Rhoads & Young (1970), in their paper on trophic group amensalism, suggest that, through their reworking of the sediment when they feed, deposit-feeding animals negatively affect the establishment of many filter-feeding species. They argue that in areas with physically unstable sediment surfaces, particles may clog filtering structures, newly settled larvae may be resuspended, and the sediment characteristics may discourage settlement of suspension-feeding larvae. However, from the present study it is obvious that filter feeders can thrive even in areas with high particle concentrations. Rhoads & Young (1970) base their hypothesis on research with active filter feeding bivalves. Amphiura filiformis is a passive filter feeder and seems not to be bothered by high concentrations of suspended particles. They can vary the number of active arms and their position above the sediment surface, and perhaps also the action of the tube feet on the arms capturing the particles. Such modifications in feeding strategy, in turbid environments, may be an advantage over most suspension-feeding bivalves. Another advantage for A.

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filiformis may be that it can switch to deposit feeding on the sediment surface (Buchanan, 1964), when the current drops to low speeds (<0.5 cm's-1, L.O. Loo, pers. comm.). As the bottom currents in the Deep Trench area not are consistent (Rodhe, 1973), suspension-feeding species may at times also feed on the food accumulated at the sediment surface. The resuspension of larvae after settlement may be reduced by the arms of A. filiformis stretching up 1 to 4 cm above the sediment surface. On densely populated bottoms such arms are likely to reduce the current speed just above the sediment surface, which would favour larval settlement and establishment. However, a dense population of A. filiformis is likely to increase the intraspecific competition between adults and post-larvae. A. filiformis allocate most of their secondary production to gonad production, which may result in heavy settlement of larvae in the adult population (SkSId et aL, 1994). To my knowledge it has not been shown that the adults eat any larvae or small animals. Ockelmann & Muus (1978) found that A. filiformis was a harmless neighbour for newly settled young Mysella bidentata. It has been observed in experiments that nematodes and acarines (Halacaridae) caught by the tube feet were immediately released to the water (L.O. Loo, pers. comm.). Thus, the larvae seem not to be eaten by A. filiformis, but a subsequent high mortality reduced the number of juveniles. The cause of the high mortality of juveniles is not known. It seems likely that A. filiformis and A. chiajei stabilize the bottom at the slopes of the Deep Trench. In the sediment profile images the top sediment is light brown, fluffy and oxidized. Deeper down, feeding voids and burrows indicate rather stable sediment conditions. However, the big sea urchin Brissopsis lyrifera, with densities of between 10 and 25 ind.m"2 and high biomasses, most probably act as a sediment destabilizer (sensu Woodin, 1983) through their bulldozing activity at some centimetres depth in the sediment. Thus, b o t h sediment stabilizers and destabilizers may persist in the same sediment and their co-occurrence has been described many times (e.g. Petersen, 1913, 1924). In an extensive investigation covering 150 stations in the North Sea (Duineveld et aL, 1987) the highest numbers recorded of Amphiura filiformis were 2124 ind.m -2. Highest densities were found at the boundaries between turbid and summer-stratified water masses, as in the Oyster Grounds (see above). Creutzberg et al. (1984), reported densities of between 400 and 2000-m-L of A. filiformis from the Oyster Grounds and a mean total biomass for that community of 13.2 g ash-free dry weight (AFDW). Using a conversion factor for A. filiformis of AFDW = 15.3% wet weight (Rumohr et aL, 1987) their biomass equalled about 86 g wet weight-m"2. This rough estimate is much lower than the biomass obtained for A. filiformis at st. D2 to D5 in the Deep Trench, and the

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abundances were also higher at st. D2, D4 and D5. At two stations (70 and 100 m) in the vicinity of the Deep Trench the biomass of the benthic communities were 110 to 128 g wet weight.m -2 in the 1970s (Josefson, 1985). This is low compared with figures obtained in this study and shows that biomass can vary greatly over short distances. The highest abundance recorded in the literature for A. filiformis is from the Saltk&llefjord on the Swedish west coast. Here, 3830 and 3934 ind.m -2 were found at two stations during a short period of high recotonisation following a large reduction in the pollution of these areas (Rosenberg, 1976). Many of these specimens were juveniles and biomass was comparatively low. These comparisons again suggest that the Deep Trench as an extremely favourable habitat for A. filiformis and some associated species. The difference between the Oyster Grounds and the Deep Trench may be that sedimentation of food in the Oyster Ground front area is largely a vertical process, whereas on the western slope of the Deep Trench the advection of organic material along the bottom is of great importance for the development of a rich fauna here. It has also been shown that phytoplankton biomass can be enhanced in the area northwest of the Deep Trench, where fronts may occur in the hydrographically dynamic mixing zone between North Sea water (Jutland Current) and Baltic water (Richardson, 1985). Part of that plant material may reach the bottom currents and be transported directly, or by resuspension processes, to the Deep Trench where most of it is apparently trapped and accumulated. Moreover, this suggests that food availability, mainly through advection along the bottom, is the primary factor supporting the high density and distribution of A. filiformis. The importance of food availability for the distribution of marine benthic populations has been reviewed by Pearson & Rosenberg (1987), and they emphasized the importance of water movement as a mediator for food availability. It has been shown from other areas of the Skagerrak and also from the northern Kattegat that A. filiformis have increased in abundance and biomass since the classical investigations by Petersen between 1910 and 1920 (Pearson et aL, 1985; Rosenberg et aL, 1987). Data from Josefson & Jensen (1992) support these findings and also that the increase occurred from 1970 onwards. All these authors suggest that the main cause may be increased food supply through eutrophication. At one of the stations sampled by Josefson & Jensen (1992) the abundance and biomass of A. filiformis reached a maximum of about 3000 ind.m -2 and close to 400 g wet weight.m -2 in the late 1980s. That station was located about 5 nautical miles west of st. D5 at 100 m depth. Do results from that single station indicate that the extreme abundance and biomass found on the slope of the Deep Trench are recent phenomena? That possibility cannot be excluded, but the A. ill#

formis in the present investigations were mostly adults, and as the growth rate is slow (3 to 4 y to reach adult size according to Muus, 1981) the present population must have been in the area for at least a few years. However, it is possible that juveniles of A. filiformis can grow faster under enriched conditions (Josefson & Jensen, 1992). Populations of A. illiformis are normally highly dominated by adults and only a few percent survive as juveniles recruiting to the adult population annually (Sk61d et al., 1994 and references therein). Thus, it cannot be excluded that higher concentrations of organic material have also been transported to the Deep Trench area during the last decade(s), and that the benthos has increased accordingly. Ockelmann & Muus (1978) have estimated that one individual of A. filiformis can oxidize an area in the sediment of about 35 cm 2 down to at least 3 cm depth. At a density of about 3000 ind.m -2, as at st. D4-D5, the total oxidized area would be in the order of 10 m2.m -2, assuming a simplified linear relationship. Josefson (1981) has investigated the depth penetration into the sediment of several species at 100 m water depth in the Skagerrak. Among the species listed in that study, and also found among the dominants in the Deep Trench, Heteromastus filiformis penetrated deepest, commonly down to at least 20 cm; Paraphinome jeffreysi was found down to 10 cm depth. As indicated in the sediment profile images, animal activity was observed down to 6 to 12 cm sediment depth, and oxic conditions were observed in sub-surface feeding voids. Thus, the infaunal activity must have a great impact on the biogeochemical processes in these sediments. Are benthic communities living on the slopes or at the bottom of the Deep Trench limited by space or by food? The space occupied by Amphiura spp. can be crudely estimated as follows, The two Amphiura species have their discs at about 3 cm below the sediment surface (Fig. 2). The disc diameter was measured of 20 individuals of both species from the western slope stations of the Deep Trench. They were 8.0 (S.D. 0.7) mm for A. filiformisand 10.0 (S.D. 0.6) mm for A. chiajeL The area these discs will cover at a densely populated station such as st. D4 is then estimated to be 0.22 m2-m°2, i.e. more than 1/5 of the area at about 3 cm depth in the sediment. However, normally two arms of each individual are stretched up to the sediment-water interface (see picture in Ockelmann & Muus, 1978, their fig. 12). Observations in thin, transparent aquaria (Rosenberg et aL, 1991), where the discs and arms could be seen, suggested that the distance between the arms at the sediment-water interface was approximately 3 cm. On the assumption that one Amphiura specimen has a direct impact (arm movements, feeding) on an area which is half that of a circular area whose diameter is the distance between the two arms, then a crude estimate of the possible area affected by these species, as exem-

STRUCTURING FACTORS FOR BENTHIC FAUNA plified for st. D4, will be 1.3 m2-m -2. Even though a species such as Mysella bidentata can live in close contact with A. filiformis, it is not likely that this is true for most other macrofaunal species. Thus, these crude estimates suggest that A. filiformis and A. chiajei together occupied a dominant part of the upper 3 to 4 cm of the sediment and that they also have a great impact on the physio--chemical conditions there down to at least 3 cm sediment depth. This suggests that the brittle stars alone may have a density-dependent impact on these bottoms and that most of the space in the upper centimetres of the sediment was occupied by them or prone to be disturbed by them. Consequently, on the western slopes, the benthic macrofauna may be space limited. The extremely high abundance and biomass, both totally and for A. filiformis at the western slope stations, must be close to the maximum that such areas can sustain for that type of benthic community. Although the numbers were higher at the deep stations, the dominant animals were generally smaller polychaetes and bivalves and, thus, the space occupied is likely to be less. It is suggested that one important factor contributing to the extreme densities of mainly Amphiura filiformis is its ability to act as both a passive suspension feeder and as a deposit feeder. When the current speed rises to above 0.5 cm.s -1 it can trap particles passing along the bottom and utilize food produced in other areas. A. filiformis can be active also in strong currents up to at least 25 cm.s 1 (L.O. Loo, pers. comm.). In periods of no or weak bottom currents, accumulation of suspended particles will occur at the bottom surface, which can be utilized by deposit feeding. Such a possible switch in feeding behaviour is likely to explain the wide distribution of A. filiformis. The distribution of A. chiajeL which is only known to be a deposit feeder (Buchanan, 1964), generally reaches highest densities at depths below those where A. filiformis dominates (Petersen, 1913). As vertical advective processes tend to attenuate with depth, when accumulation rate increases such bottom habitats should favour deposit feeders such as A. chiajeL Thus, the difference in distribution of these two Amphiura species (A. filiformis predominating at depths between 15 and 40 m, and A. chiajei at depths between 40 and 100 m (Petersen, 1924)) is not a matter of depth per se, but related more to hydrodynamic process and food availability. Food availability does not seem to limit the populations on the slope. The high flux of organic material down the slope, at least intermittently, promotes thriving benthic communities. This strongly suggests that most other benthic communities with similar species composition, but with significantly lower abundance and biomass, could be limited by food availability. Thus, it indicates that benthic soft-bottom communities of this type (characterized by Amphiura spp.) are generally food limited. This would include most soft-bottoms from 15 to below 100 m depth in the

315

Skagerrak, the Kattegat and the North Sea, as judged from animal community distributions and their abundance and biomass (e.g. Josefson, 1985; Duineveld et aL, 1987; Petersen, 1913, 1924). Lower densities may also partly be a consequence of greater competition, predation or other disturbances such as bottom trawling. However, predation is unlikely to be a dominant factor, because predation on A. filiformis is practically confined to nipping off the arms without significantly affecting the long-term population stability (SkSId et aL, 1994). Neither does trawling appear to be an important factor because A. filiformis populations have been shown to increase rather than to decrease in some areas with trawling (Josefson, 1990). As competition through negative interactions does not seem to depress the total density and biomass of the communities on the slopes of the Deep Trench, it is not clear why such interactions should have very different impacts on similar communities elsewhere, unless they compete for food. In conclusion, bottoms with excess food availability can harbour rich benthic communities. This suggests that the benthic fauna in many other areas is food limited. Acknowledgement.--I thank Birthe Hellman, Sture Ottosson and Rod Stevens for technical assistance. Many thanks to Robert Diaz, Lars-Ove Loo, Tom H. Pearson, Johan Rodhe, Mattias Sk6ld and two anonymous referees for constructive criticism of the manuscript. This work was supported by the Swedish Natural Science Research Council (contract B-BU 3294-308) and the Swedish Environment Protection Agency (contract 26341). 6. REFERENCES Abacus Concepts, 1989. SuperANOVA. Abacus Concepts, Inc., Berkeley, California, USA: 1-322. Arntz, W.E., D. Brunswig & M. Sarnthein, 1976. Zonierung von Mollusken und Schill im Rinnensystem der Kieler Bucht (Westliche Ostsee).--Seckenb. mar. 8:198-269. Bray, J.R. & J.T. Curtis, 1957. An ordination of the Upland forest communities of Southern Wisconsin.--Ecol. Monogr. 27: 325-349. Buchanan, J.B., 1964. A comparative study of some features of the biology of Amphiura filiformis and Amphiura chiajei (Ophiuroidea) considered in relation to their distribution.--J, mar. biol. Ass. UK 44: 565-576. Butman, C.A., M. Fr~chette, W.R. Geyer & V.R. Starczak, 1994. Flume experiments on food supply to the mussel Mytilus edulis L. as a function of boundary-layer flow.--Limnol. Oceanogr. 39:1755-1768. Cheng, I.-J., J.S. Levinton, M. McCartney, D. Martinez & M.J. Weissburg, 1993. A bioassay approach to seasonal variation in the nutritional value of sediments.--Mar. Ecol. Prog. Ser. 94: 275-285. Clough, L.M. & G.R. Lopez, 1993. Potential carbon sources for the head-down deposit-feeding polychaete Heteromastus filiformis.--J, mar. Res. 51:595-616. Cramer, A., 1990. Seasonal variation in benthic metabolic activity in a frontal system in the North Sea. In: M. Barnes & R.N. Gibson. Trophic relations in the marine environment. Aberdeen Univ. Press, Aberdeen: 54-76.

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population.--Mar. Ecol. Prog. Ser. 183: 81-90. Van Weering, T.C.E., G.W. Berger & E. Okkels, 1993. Sediment transport, resuspension and accumulation rates in the northeastern Skagerrak.--Mar. Geol. 111: 269-285. Woodin, S., 1983. Biotic interactions in marine sedimentary environments. In: M.J.S. Tevesz & P.L. McCall. Biotic interactions in recent and fossil benthic communities. Plenum Press: 3-38. (accepted 21 June 1995)