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Depth Correlated Benthic Faunal Quantity and Infaunal Burrow Structures on the Slopes of a Marine Depression
Estuarine, Coastal and Shelf Science (2000) 50, 843–853 doi:10.1006/ecss.2000.0614, available online at http://www.idealibrary.com on
Depth Correlated Benthic Faunal Quantity and Infaunal Burrow Structures on the Slopes of a Marine Depression R. Rosenberga, H. C. Nilsson, B. Hellman and S. Agrenius Department of Marine Ecology, Go¨teborg University, Kristineberg Marine Research Station, 450 34 Fiskeba¨ckskil, Sweden Received 6 December 1999 and accepted in revised form 19 February 2000 In the northern part of the Kattegat, western Sweden, a series of marine depressions remain since the last glaciation. One of these, the well-oxygenated Alkor Deep, is about 3 km long and 800 m wide and with a depth of 138 m. Random depth-stratified sampling was made along four transects on the slopes including benthic macrofauna (0·1 m2 grab samples) and sediment profile imaging. A significant positive correlation was found between depth and the faunal variables abundance and biomass. Deposit feeders such as Maldane sarsi, Heteromastus filiformis and Abra alba were among the dominants and may have been supported by down-slope advected organic material. In many images, pockets and extensive burrows were seen in the sediment that appeared to be constructed by the crustaceans Calocaris macandreae and Maera loveni. The ecological significance of their irrigation of the sediment is discussed. Due to the faunal activity deep down in the sediments of the slopes, the mean apparent redox potential discontinuity (RPD) was found as deep as between 8·0 and 11·3 cm depth, and RPD was significantly positively correlated with water depth. On the slopes there appears to be a balance between the input of organic material and the capacity of the benthic organisms to assimilate that carbon. 2000 Academic Press Keywords: sediment profile imaging; bioturbation; deposit feeder; Calocaris; Maera; Melinna; Kattegat
Introduction In the classical papers by Petersen (1913), Thorson (1957) and Molander (1963) it was shown that bottom fauna communities could be homogeneous over large areas and that dominant species appeared repeatedly and characterized these communities. A rather uniform pattern in distribution may, however, be interrupted or gradually changed when environmental conditions change. The time and scale at which a disturbance may occur will have an impact on the faunal succession and structure (Zajac & Whitlatch, 1982; Zajac et al., 1998). It has been demonstrated that hydrodynamically enhanced inputs of food to the benthos can change the faunal composition over short distances (Creutzberg et al., 1984) and locally increase the abundance and biomass significantly (Rosenberg, 1995). These two latter studies support the concept of a strong pelagicbenthic coupling (Josefson & Conley, 1997) and the importance of food availability as a major structuring factor of marine benthos (Pearson & Rosenberg, 1987). a
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Pearson and Rosenberg (1978) and Rhoads and Germano (1982) demonstrated that benthic communities respond in a predictable way to changes in organic input and physical disturbance. Their models also suggested that an increased input of organic carbon would result in an increase of deposit-feeding animals relative to suspension feeders. At a moderate input of organic matter, the vertical depth distribution of infauna in the sediment could increase. Josefson (1981), Dauwe et al. (1998) and Weston (1990) found that a faunal activity down to at least 20 cm within the sediment could occur in the Skagerrak, the North Sea and in coastal areas in the Pacific, respectively. The models cited above on infaunal distribution are useful descriptors of benthic community succession in relation to disturbance. For a thorough understanding of functional aspects, information about faunal bioturbation, irrigation, interaction, and their effects on redox conditions and chemical element fluxes and transformations are needed. The Kattegat is a shallow sea with a mean depth of 23 m (Svansson, 1975). However, a deep channel— the Kattegat Channel System—with depths of around 80 to 100 m is an extension southwards of the 2000 Academic Press
844 R. Rosenberg et al.
F 1. The study area. (a) shows the sampling area, the Alkor Deep (Ad), and also the Deep Trench (Dt) and the Norwegian Trench (Nt), (b) is a detailed map of the Alkor Deep with depth contours and sampling transects (solid lines), (c) is a depth profile along the transect from south-east towards north-west.
Norwegian Trench and the Deep Trench in the Skagerrak (Figure 1). The channel system contains some localized, deep depressions, where the environmental conditions for the benthic fauna are suggested to be extraordinary compared with the surrounding bottoms. These depressions were probably formed as a postglacially influenced periglacial melt-water channel about 15 000 to 11 000 years ago (Ulrich & Eisele, 1993). The present study focused on the Alkor Deep, which is about 3 km long, 800 m wide and with a maximum depth of 138 m. Water temperature and salinity deeper than 70 m were recorded at 4 to 6 C and 33·5 to 34·2 (using the Practical Salinity Scale), respectively (Tarling et al., 1998). The surficial sediments in the deeper part of this depression was found to be of recent origin, and the sedimentation rate suggested to be lower than the 3·2 cm yr 1recorded in an adjacent depression, the Littorina Deep (Blanz, 1992). The deepest part of the depression and the slopes are characterized by fine sediments, whereas on the flatter part, at about 40 m, sand may predominate (Nordberg et al., 1999). Blanz (1992) recorded no methane gas in the sediment in the Alkor Deep and suggested that bottom currents keep some of these depressions rather intact. Currents in the deeper part of the Alkor Deep have been recorded to flow mainly along the main north-south axis [Figure 1(b)] and frequently exceed 10 m s 1 (Buchholz et al., 1995). Another interesting observation is that krill (Meganyctiphanes norvegica) occupies a southern refuge in its distribution, towards more brackish water of Baltic origin, in these depressions (Tarling et al., 1998).
The aim of this study was to investigate the benthic faunal composition and their sedimentary habitat on the slopes and deep bottom of the Alkor Deep. We hypothesize that the steep slopes and the presumably associated sediment transport will represent a disturbance to suspension feeders, but instead promote deposit feeders by intermittent deposition and resuspension of organic material. Signs of infaunal activity in the sediment and the apparent redox profile discontinuity were analysed in images obtained by a sediment profile camera (e.g. Rhoads & Germano, 1986). The same methods were used in a nearby area, the Deep Trench (Figure 1), where bottom-near currents mediated a horizontal transport of food particles and where an extremely high sedimentation rate occurred on one side of the slope (Rosenberg, 1995). In the present study we show that the faunal abundance and biomass and redox conditions on the slopes of the Alkor Deep increased with depth. This is part of a joint research project where Nordberg et al. (1999) have analysed foraminiferans in relation to hydrographic conditions and Rodhe et al. (1998) studied current regimes. Material and methods Sampling was carried out on 19 to 22 September 1994. Sediment profile images (SPIs) and grab samples of infauna were randomized in 20 m depth intervals from the slopes down to the deepest part of the Alkor Deep (Figure 1). Within these depth strata, the sample sites were distributed around four transects
Benthic faunal quantity and infaunal burrow structures 845
800
(a)
60
(b)
2
R2 = 0.34 Biomass (g 0.1 m–2)
Abundance (0.1 m2)
R = 0.53 600
400
200
0 16
50 40 30 20 10 0
(c)
(d) 2
R = 0.46
13
R2 = 0.33
BHQ-index
RPD (cm)
12
8
4
0 40
11 9 7
60
80 100 Depth (m)
120
140
5 40
60
80 100 Depth (m)
120
140
F 2. Linear positive correlations with depth and abundance (a), biomass (b), apparent Redox Profile Discontinuity (RPD) (c), and Benthic Habitat Quality (BHQ) index (d) in the Alkor Deep.
and numbered according to compass directions from Alkor Deep, NE (25), SE (135), SW (205) and NW (315) [Figure 1(b)]. The depth strata were 80–99, 100–119 and 120–138 m for all four transects. In the NW and SE directions the bottom levelled off at 40 m and here also the depth strata 40–59 and 60–79 were sampled. The samples in the different strata were named after transect directions and shallowest depth of stratum, e.g. NW40, NW60, etc, and the deepest stratum is named A120. Four in situ Sediment Profile Images (SPIs) were taken in each stratum, except in stratum NE80 where the camera failed. Images were taken through a prism (30 cm long, 22 cm wide; see Rosenberg & Diaz, 1993). The contrast of the colour of the sediment was digitally enhanced in Adobe Photoshop 4.0. Depth of mean apparent Redox Potential Discontinuity (RPD; Fenchel & Riedel, 1970) was analysed in NIH image 1·6. The Benthic Habitat Quality (BHQ) index was calculated in each image, where (a) the sediment surface and (b) sub-surface structures and (c) the apparent RPD were parameterized. The BHQ index range between 0 and 15, where low indices indicate poor faunal conditions in the sediment and values >10 stands for later stage seral communities (Nilsson & Rosenberg, 1997, 2000).
Infauna was collected by taking four samples in each stratum with a 0·1 m2 Smith-McIntyre grab, totally 56 samples. The grab was filled with sediment at all occasions and penetrated to a maximum depth of 18 cm. The sediment was sieved through a 1 mm mesh and the fauna was picked out gently and preserved in 70% ethanol. Infaunal similarity was analysed by applying the Bray-Curtis similarity coefficient to √√-transformed abundance and biomass data of all taxa; based on this index the samples were analysed by MultiDimensional Scaling (MDS; Clark & Warwick, 1994). Correlations between sampling depth and fauna and sediment parameters were analysed by simple linear regression. Statistical significance of regressions was tested by Kendall’s rank correlation coefficient (Sokal & Rohlf, 1981). Results Faunal composition and quantity A significantly positive correlation (R2 =0·53, P<0·001) was found between depth and mean total abundance of fauna [Figure 2(a)]. At depth strata between 40 and 79 m, mean abundance per 0·1 m2
846 R. Rosenberg et al.
was <200, and in the deepest strata abundance was >400 (Table 1). Similarly, a significant positive correlation (R2 =0·34, P<0·001) was found between depth and mean biomass [Figure 2(b)]. In the depth strata 40 to 79 m, mean biomass per 0·1 m2 was 5·8 to 19·2 g wet weight and in all deeper strata it was higher, between 19·9 and 37·1 g. Mean number of taxa per 0·1 m2 in the area was between 24 and 38 with no depth correlation. Total number of taxa was 150. Significantly negative correlations between Shannon-Wiener diversity H (R2 =0·49, P<0·001) and evenness J (R2 =0·53, P<0·001) and depth were recorded. Most of the three dominant species in each depth strata were present over the whole area but with highest numbers at greater depths (Table 1). The tube-building polychaete Maldane sarsi had high abundances in several of the deep strata, but was almost absent along the SE-transect. The head-down deposit-feeding polychaete Heteromastus filiformis was found in highest numbers on the slopes. The surface deposit-feeding bivalve Abra nitida had a rather homogeneous distribution over the whole area varying in numbers between 13 and 84 per 0·1 m2. Most of the species in the area were surface or sub-surface deposit feeders. If the brittlestar Amphiura filiformis, which can be both a suspension feeder and a deposit feeder (Loo et al., 1996), was excluded from a comparison of feeding groups in the Alkor Deep, about 90% of the individuals would be classified as deposit feeders, about 10% as predators and almost no suspension feeders. Most of the deposit feeders were feeding on the sediment surface. The crustaceans Maera loveni and Calocaris macandreae are known to dig extensive burrows in muddy sediment (Atkinson et al., 1982; Nash et al., 1984). They were present in most samples (Table 1). The small epifaunal brittlestar Ophiura affinis occurred in numbers between 5 and 27 per 0·1 m2 at depths greater than 100 m. Several individuals of the peculiar ‘ mast ’ building crustacean Dyopedos monacanthus were found in the deep strata A120 and NW100. The hagfish Myxine glutinosa was captured in several grabs from depths below 80 m, but was excluded from this presentation. Dominants in biomass were the heart urchin Brissopsis lyrifera (0–11·5 g wet wt per 0·1 m2) and the brittlestars Amphiura chiajei (0·3–4·8 g) and A. filiformis (0-8·6 g). Multivariate analyses of abundance and biomass showed similarities within the strata SE40, NW40 and SE60; for abundance also for NW60 and SE80 (Figure 3). The deeper strata d80 m generally grouped together and were separate from the shallow strata. Thus, a difference in faunal composition was found
between the shallow stations and for those on the slopes and bottom. Sediment and sediment profile images The organic carbon content in the upper 2 cm of the sediment in the Alkor Deep varied between 2·1 and 2·5% of the dry weight (Table 1; data from Nordberg et al., 1999). Mean penetration of the prism into the sediment was between 10·6 and 20·7 cm (Table 1), and increased significantly with depth (R2 =0·23, P<0·01) indicating softer sediments in deeper water. Burrow structures and voids were seen in almost all images and infauna in about half of them. In many images, oxic voids were found deeper than 10 cm in the sediment with a mean maximum depth of 18·8 cm, indicative of deep feeding and irrigation activity. Depth of mean apparent RPD was, with one exception, >3 cm and in some strata >10 cm. Apparent RPD was significantly positively correlated with depth [R2 =0·46, P<0·001; Figure 2(c)]. These observations are clear indications of an extensive faunal activity deep within the sediment. Activity of infauna was seen in all images from the Alkor Deep. Six SPIs are presented from different depths (Figure 4). The rust-brown colour is indicative of the oxidized sub-oxic zone. The sediment is reworked in the upper centimetres. The large burrows and tunnels observed in the images from 60 m and deeper were probably made by Calocaris macandreae and Maera loveni. The image A120 shows two large burrows extending down towards the bottom of the picture, which seem to lead even further down in the sediment. An arm of a brittlestar is seen in the middle of the left burrow. In image NE100 several polychaetes are visible that are suggested to be head-down feeding Heteromastus filiformis. Similarly, in image SW80, SE80 and SE60 extensive burrow systems are visible, and also indications of vertical burrows or tubes that in some cases extend all the way to the bottom of the images. Some of these are suggested to indicate the presence of Melinna cristata, H. filiformis and Maldane sarsi. In the SE44 image the sediment surface is uneven with sand at the top and clay below. The surface is reworked and the pockets could be made of Abra nitida or Amphiura filiformis. Only few tubes and no other structures are seen above the sediment surface. Mean BHQ indices varied between 8·0 and 11·3, and a significant positive correlation (R2 =0·33, P<0·001) was found with depth [Figure 2(d)]. At depths below 80 m, individual images always had BHQ indices d9, and the mean indices in each of these deeper strata were >10. This is indicative of an
a
From Nordberg et al. (1999).
Dominant species Maldane sarsi Heteromastus filiformis Abra nitida Amphiura filiformis Amphiura chiajei Leucon nasica Spiophanes kroeyeri Chaetozone setosa Alvania testae Deep burrowing species Maera loveni Calocaris macandreae Community variables Mean total abundance Mean total biomass Mean no. of taxa Diversity H Evenness J Sediment measurements Mean penetration Mean RPD Mean BHQ Max depth of tunnel or void Organic carbon (%)a
Average depth (m)
2 + 1 412 28·3 27 2·3 0·7 16·0 9·3 11·5 15·3 2·4
3 1 449 31·6 33 2·4 0·7 20·2 10·2 10·7 18·8 2·5
99 66 78 34 22 36
NE 100 107
81 72 80 49 25 29 6 3
A 120 126
20·0 10·8 10·8 17·0 2·4
463 37·1 32 2·4 0·7
2 +
75 70 80 73 14 27 7 4
SW 100 113
20·7 12·0 11·0 16·2 2·3
456 28·3 35 2·4 0·7
2 1
113 64 80 45 15 11 9 3
NW 100 112
13·9 7·9 11·0 12·7 2·3
584 29·4 34 1·9 0·5
1 +
311 49 76 9 15 10 1
SE 100 110
2·3
258 24·6 28 2·4 0·7
+ 2
1 88 31 30 10 20 6 3
NE 80 88
19·1 9·6 11·0 14·0 2·3
335 27·5 30 2·3 0·7
1
105 69 36 8 17 17 9
SW 80 92
18·5 5·9 11·3 16·8
529 33·4 34 2·4 0·7
1 1
124 77 84 65 14 11 6 4 +
NW 80 98
12·7 3·6 10·8 8·9 2·3
204 19·9 29 2·4 0·7
1 1
+ 29 61 35 7 5 12 4
SE 80 91
14·0 4·1 7·0 12·8
147 19·2 30 2·7 0·8
1 1
2 23 26 3 12 8 12 4 2
NW 60 76
17·8 6·6 9·3 12·2 2·4
117 7·6 24 2·5 0·8
+
+ 34 13 3 5 11 8 7
SE 60 75
13·2 3·0 9·3 7·4
196 17·1 37 2·9 0·8
+
1 25 32 10 20 8 2 2 5
NW 40 46
10·6 2·6 8·0 8·4 2·1
159 5·8 38 3·1 0·9
1
+ 2 35 6 1 1 5 11 12
SE 40 51
T 1. Alkor Deep. Mean benthic faunal (per 0·1 m2) and sediment data at the different depth strata; (a) abundance of the 3 dominant species at each station, and (b) of deep burrowing crustaceans, (c) community variables, and (d) measurements of sediment profile imaging. +indicates single occurrence
Benthic faunal quantity and infaunal burrow structures 847
848 R. Rosenberg et al. Abundance
Stress = 0.20
Biomass
Stress = 0.20
NW40
NW40
SE40 SE40 SE60
NW60 SE80 SE80
SE60
F 3. Plots showing the faunal similarities as Multi-Dimensional Scaling (MDS) based on abundance (left) and biomass (right) data. Some depth strata that group together are encircled.
equilibrium successional stage III benthic community (Nilsson & Rosenberg, 1997). Discussion Benthic community distribution The community structure of the benthic fauna in the Alkor Deep is related to depth. In each of the two shallow depth strata at 40 to 59 and 60 to 79 m, the faunal compositions were rather uniform (Figure 3). One reason for the differences in community structure could be that at depths of 46 to 67 m patches of sand occurred (Nordberg et al., 1999), which could have affected the faunal composition. In addition, larger areas were sampled at the shallower depths compared to on the slopes with a possible greater variation between samples as shown in the MDS-plot. All deeper stations grouped together in the MDS-plot, and the faunal structure was separated from those above 80 m depth. Distribution of foraminiferans was investigated during the same survey as the present (Nordberg et al., 1999). The authors of that study concluded that the species composition of foraminiferans showed a discontinuity in distribution at about 80 m water depth. They attributed this to similarities in deep-water hydrography, and they concluded that the Alkor Deep does not have stagnant water but is connected to the deeper areas further north. In the present study, the benthos on the slopes and in the deepest part had higher abundance and biomass
compared with the shallower and flatter area. We suggest that these gradual increases in faunal quantity on the slopes are mainly due to differences in bottom current mediated down-slope transport of organic particles. Availability of food in surplus for the benthos has been shown in this sea area to enhance faunal numbers and biomass (Josefson & Jensen, 1992; Rosenberg, 1995). Deposit feeding and particle transport Approximately 90% of the animals on the slopes of Alkor Deep feed on the particles deposited on, or in, the sediment. Little is known about the ecological effects of sediment transport and deposition rates on deposit-feeding animals (Nowell et al., 1989). It has been demonstrated that near-bottom currents are important for lateral particle flux and for the supply of food for benthic animals (Thomsen et al., 1995). Resuspension of particles is determined by water flow rate, bottom shear velocity and bottom roughness (Jumars, 1993; Graf & Rosenberg, 1997). Benthic animals can either stabilize or destabilize sediments and thus have a direct impact on the erodibility (Rhoads & Boyer, 1982; Jumars & Nowell, 1984). It has been demonstrated that spionid polychaetes respond positively to moderate sediment transport by increased feeding and fecal pellet production (Dauer et al., 1981; Nowell et al., 1989). Some species that are sub-surface feeding may also be able to collect food particles on the surface (Levin et al., 1997) and
Benthic faunal quantity and infaunal burrow structures 849
F 4. Sediment profile images from the strata A120, NE100, SW80, SE80, SE60 and SE40. The contrasts are enhanced to better visualize burrows, voids and the Redox Potential Discontinuity (RPD). The rust-brown colour indicates the oxidized sub-oxic zone. Burrow structures that appear to be constructed by Calocaris macandreae and Maera loveni are clearly seen in the images from 60 m and deeper. Several polychaetes, probably Heteromastus filiformis, are seen in the NE100 image. The vertical scale is centimetres, and the black rectangle masks reflections of the flash.
may take advantage of this when particles transported down-slope can be captured. Other deposit feeders may be dependent on the rate of sedimentation into their feeding depressions (Nowell et al., 1984). Graf and Rosenberg (1997) showed that biodeposition of particles on the sediment surface are of significant quantitative importance. The above information about deposit feeders demonstrates that some species are able to adjust to variations in sediment transport and that this transport can provide an additional food supply. Thus, the increases in numbers and biomass of the infauna on the slopes of the Alkor Deep are suggested to be a response to down-slope transport of sediment-associated food particles.
The impact of infaunal bioturbation and biodeposition on resuspension has been documented, especially for deposit feeders, e.g. by Davis (1993) and Graf and Rosenberg (1997). Deposit feeding accounts for most bioturbation of particles in the sediment because deposit feeders feed at a high rate and use separate sites of ingestion and egestion (Jumars & Wheatcroft, 1989). The sediment surface observed in the SPIs always showed signs of infaunal activity, and large-scale erosions seem not to occur on the slopes or deep bottoms in this area. The disturbance caused by the activity of the deposit feeders may, together with down-slope sediment transport, create a physical disturbance unsuitable for
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suspension feeders and even some deposit feeders. For example, Hollertz et al. (1998) have shown that activity of Brissopsis lyrifera can negatively affect the growth of Amphiura chiajei. Moreover, active burrowing crustaceans my destabilise the sediment when feeding and moving, which is likely to have a negative impact on some sessile and stationary animals such as tube builders (Brenchley, 1981). Comparisons of faunal distribution In the deepest part of the Norwegian Trench in the Skagerrak [Figure 1(a)], the composition of the macrofauna showed a discontinuity at about 400 m (Rosenberg et al., 1996). Josefson (1985) found major divisions in faunal community distribution between the depth intervals 40–200, 200–360 and 360–650 m in the eastern Skagerrak. Comparisons showed that abundance was lower, and biomass much lower, both on the slopes and in the deep part of the Norwegian Trench compared with the Alkor Deep slopes. The organic content in the surface sediments were similar in both areas, but due to the difference in water depth, the carbon was probably more refractory in the Norwegian Trench. The benthic fauna in the Deep Trench in the south-east Skagerrak [Figure 1(a)] was studied by Rosenberg (1995). Both the western slopes and the deeper bottoms at 100 m of this trench had a macrofauna abundance that was higher, or much higher, at all stations (up to 13 600 ind m 2). Also the biomass was higher in the Deep Trench than in Alkor Deep on several stations, and so was the organic content in the surficial sediment (2·8 to 3·4%). The author explained the extremely high abundance and generally high biomass in the Deep Trench to be caused by a great transport of organic particles in the bottom-near water, and an extremely high sedimentation rate. It was suggested that the animals were not limited by food but rather by space. Thus, hydrodynamic processes most probably advected food particles that optimised the conditions for the benthic fauna. Faunal activity deep in the sediment The SPI complements the information about the sedimentary habitat that is usually obtained by taking grab samples and analysing the fauna. SPIs give an in situ view of the sediment redox conditions and faunal activity (Rhoads & Germano, 1986). Parameterization of the information has proven to be useful, and the Benthic Habitat Quality (BHQ) index is related to the successional stages in the Pearson-
Rosenberg (1978) model (Nilsson & Rosenberg, 1997, 2000). The BHQ indices were >10 on the slopes and are indicative of late successional stage communities. Thus, these types of benthic communities have most probably been present in the area for decades, which suggests, in agreement with Nordberg et al. (1999), that the bottoms of the Alkor Deep are well flushed. In 1995, the total organic content in the surficial sediment along the Swedish Skagerrak coast was found to be between 0·9 and 3·7% of the dry weight with a mean of 2·5% (Cato, 1997). In comparison with that mean and percentages given above for the Norwegian Trench and the Deep Trench, the sediments on the slopes in Alkor Deep (Table 1) seem not to have an enhanced content of carbon. The mean of the apparent RPD is very high in comparison with other similar studies in coastal areas on the U.S. east coast (Grizzle & Penniman, 1991; Schaffner et al., 1992; Valente et al., 1992), the Baltic (Bonsdorff et al., 1996), and the Deep Trench (Rosenberg, 1995), the Norwegian Trench (Rosenberg et al., 1996) and fjords in the Skagerrak (Nilsson & Rosenberg, 1997, 2000). This deep apparent RPD is a consequence of faunal activity down to great depths in the sediment, and suggests that the organic carbon is not accumulated but rather assimilated. It is likely that the deep-burrowing species Calocaris macandreae and Maera loveni contribute to the oxygenation of the sediment and the mineralization of carbon (Forster & Graf, 1992). Many species are likely to live in close contact with the burrows constructed by these species (Dauwe et al., 1998) and contribute to the breakdown of organic material. Several individuals could be in the meiofaunal size range, which were not included in this study. The mean depth of the apparent RPD in the Deep Trench was much lower (<5 cm) than in the Alkor Deep. This in combination with the comparatively higher organic content in the sediment implies that the transport of organic material to the bottoms in the Deep Trench was higher than in the Alkor Deep or took longer to mineralize. Deep burrowing crustaceans like C. macandreae and M. loveni and the rather large tube-building polychaete Melinna cristata were missing in areas with high organic deposition in the Deep Trench. The comparatively lower abundance of A. filiformis and the associated small bivalve Mysella bidentata in the Alkor Deep compared with the Deep Trench could be caused by interspecific disturbance of these tunnel-building crustaceans, or that the amount of horizontally advected food was less. In summary, we conclude that in the Alkor Deep there appears to be a balance between input of organic material and the capacity of the benthic organisms to
Benthic faunal quantity and infaunal burrow structures 851
assimilate that carbon. This balance seems to have persisted for a long time, probably decades, as the benthic fauna was assessed to be in an equilibrium successional stage. The maximum depth where tunnels and voids were seen in the SPIs were 18·8 cm and in most cases below 10 cm in the sediment. In some samples signs of faunal activity was close to the depth of mean penetration of the prism. Thus, these large burrow structures were common over the whole area and most pronounced on the slopes. Dauwe et al. (1998) showed that infauna occurred down to about 20 cm in the sediment at three stations in the North Sea and the Skagerrak. They also recorded the largest individual sizes and the deepest distribution where the organic matter was of intermediate quality and quantity. Estimates of tunnel areas and volumes in the sediment The bioturbation and biodeposition in the Alkor Deep was not measured, but it is probably significant (see below) and important for the rate of mineralization. It appears from the grab samples that the deep, large burrow structures observed in the SPIs are made by the mud shrimp Calocaris macandreae and the amphipod Maera loveni (Table 1). Their burrowing activity and tunnel constructions are described in papers by Atkinson et al. (1982) and Nash et al. (1984) and some details from those publications are summarized below. Both species spend almost all time in their burrows. These are initially U-shaped and later elaborated with vertical tunnels and further openings to the surface. The tunnels of C. macandreae descend deep down into the sediment and frequently form a second level of horizontal tunnels. The tunnel diameter has been measured at 14 to 19 mm for C. macandreae, and on average 19 mm for M. loveni. The maximum depths for both species can in some cases extend vertically beyond 20 cm. Thus, it seems not possible to separate the burrow systems into species in the SPIs. The variations in sediment tunnel area and volume in burrows of C. macandreae and M. loveni were found to be large, but crude averages of tunnel areas occupied by single individuals could be 0·1 and 0·05 m2, with volumes corresponding to 0·5 and 0·1 l, respectively (Atkinson et al., 1982; Nash et al., 1984). At depths below 80 m in the Alkor Deep every square metre may be occupied by 10 C. macandreae and 10 M. loveni (Table 1). With such assumptions, the two crustaceans can have tunnels in the order of 1·5 m2 with a volume of 6 l per m2. Tunnels and voids were seen in most of the SPIs from below 60 m water depth. These descended to depths below 12 cm, and
as these structures frequently were large, they were probably tunnels made by C. macandreae and M. loveni. Their irrigation of at least parts of the tunnel system will be beneficial for other infaunal organisms (Schaffner, 1990) and have significant effects on the geochemistry in the sediment (Gilbert et al., 1998). The bioturbation rates of these animals have not been assessed, but records from other areas suggest that it can be high for many species (Lee & Swartz, 1980; Diaz & Schaffner, 1990). The two crustaceans were collected in most of the grab samples, but their abundances were most likely underestimated as the grab only was biting down to a maximum depth of 18 cm and animals deeper down or on the outside of each half of the grab were not collected. It seems therefore that the bottoms of the Alkor Deep are extensively bioturbated, especially below about 80 m water depth.
Acknowledgements We thank the crew on RV Skagerak and Dr Mattias Sko¨ ld for technical assistance; Dr Kjell Nordberg for comments of the manuscript; and the Swedish Natural Science Research Council and the Go¨ teborg University Marine Research Centre for financial support.
References Atkinson, R. J. A., Moore, P. G. & Morgan, P. J. 1982 The burrows and borrowing behaviour of Maera loveni (Crustacea: Amphipoda). Journal of Zoology, London 198, 399–416 Blanz, T. 1992 Sedimetologische und sedimentphysikalische Eigenshaften holoza¨ ner Sedimentkerne aus der Alkor- und Littorina-Tiefe/no¨ rdliches Kattegat. Meyniana 44, 75–95 Bonsdorff, E., Diaz, R. J., Rosenberg, R., Norkko, A. & Cutter, G. R. J. 1996 Characterization of soft-bottom benthic habitats of the A r land Islands, northern Baltic Sea. Marine Ecology Progress Series 142, 235–245 Brenchley, G. A. 1981 Disturbance and community structure: an experimental study of bioturbation in marine soft-bottom environments. Journal of Marine Research 39, 767–790 Buchholz, F., Buchholz, C., Reppin, J. & Fischer, J. 1995 Diel vertical migrations of Meganyctiphanes norvegica in the Kattegat: Comparison of net catches and measurements with Acoustic Doppler Current Profiles. Helgola¨ nder Meeresuntersuchungen 49, 849–866 Cato, I. 1997 Sedimentological investigations of the Bohus Coast 1995—The Coast Water Monitoring Program of Go¨ teborg and Bohus County, and changes after 1990. Sveriges Geologiska Underso¨ kningar 95, 25–154 Clark, K. R. & Warwick, R. M. 1994 Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth Marine Laboratory, Plymouth. Creutzberg, F., Wapenaar, P., Duineveld, G. & Lopez Lopez, N. 1984 Distribution and density of the benthic fauna in the southern North Sea in relation to bottom characteristics and hydrographic conditions. Rapport et Proces-verbaux des Reunions, Conseil International pour l’Exploration de la Mer 183, 101–110
852 R. Rosenberg et al. Dauer, D. M., Maybury, C. & Ewing, R. M. 1981 Feeding behaviour and general ecology of sveral spionid polychaetes from the Chesapeake Bay. Journal of Experimental Marine Biology and Ecology 54, 21–38 Dauwe, B., Herman, P. M. J. & Heip, C. H. R. 1998 Community structure and bioturbation potential of macrofauna at four North Sea stations with contrasting food supply. Marine Ecology Progress Series 173, 67–83 Davis, W. R. 1993 The role of bioturbation in sediment resuspension and its interaction with physical shearing. Journal of Experimental Marine Biology and Ecology 171, 187–200 Diaz, R. J. & Schaffner, L. C. 1990 The functional role of estuarine benthos. In Perspectives on the Chesapeake Bay, 1990 (Haire, M. & Krome, E. C., eds), Advances in Estuarine Sciences, Chesapeake Research Consortium, Gloucester, pp. 25–56 Fenchel, T. M., Riedel, R.J. 1970 The sulfide system: a new biotic community underneath the oxidized layer of marine sand bottoms. Marine Biology 7, 255–268 Forster, S. & Graf, G. 1992 Continuously measured changes in redox potential influenced by oxygen penetrating from burrows of Callianassa subterranea. Hydrobiologia 235/236, 527–532 Gilbert, F., Stora, G. & Bonin, P. 1998 Influence of bioturbation on denitrification activity in Mediterranean coastal sediments: an in situ experimental approach. Marine Ecology Progress Series 163, 99–107 Graf, G. & Rosenberg, R. 1997 Bioresuspension and biodeposition: a review. Journal of Marine Systems 11, 269–278 Grizzle, R. E. & Penniman, C. A. 1991 Effects of organic enrichment on estuarine macrofaunal benthos: a comparison of sediment profile imaging and traditional methods. Marine Ecology Progress Series 74, 249–262 Hollertz, K., Sko¨ ld, M. & Rosenberg, R. 1998 Interactions between two deposit feeding echinoderms: the spatangoid Brissopsis lyrifera (Forbes) and the ophiurid Amphiura chiajei Forbes. Hydrobiologia 375/376, 287–295 Josefson, A. B. 1981 Persistence and structure of two deep macrobenthic communities in the Skagerrak (west coast of Sweden. Journal of Experimental Marine Biology and Ecology 50, 63–97 Josefson, A. B. 1985 Distribution of diversity and functional groups of marine benthic infauna in the Skagerrak (eastern North Sea)—can larval availability affect diversity? Sarsia 70, 229–249 Josefson, A. B. & Conley, D. J. 1997 Benthic response to a pelagic front. Marine Ecology Progress Series 147, 49–62 Josefson, A. B. & Jensen, J. N. 1992 Growth patterns of Amphiura filiformis support the hypothesis of organic enrichment in the Skagerrak-Kattegat area. Marine Biology 112, 615–624 Jumars, P. A. 1993 Consepts in Biological Oceanography: An Interdisciplinary Primar. Oxford University Press, New York, 348 pp. Jumars, P. A. & Nowell, A. R. M. 1984 Effects of benthos on sediment transport: difficulties with functional grouping. Continental and Shelf Research 3, 115–130 Jumars, P. A. & Wheatcroft, R. A. 1989 Responses of benthos to changing food quality and quantity, with a focus on deposit feeding and bioturbation. In Productivity of the ocean: Present and Past (Berger, W. H., Smetacek, V. S. & Wefer, G., eds), J. Wiley & Sons, New York pp. 235–253 Lee, H. I. & Swartz, C. 1980 Contaminents and Sediments. In Biological Processes Affecting the Distribution of Pollutants an Marine Sediments. Part II. Biodepostion and bioturbation. (Baker, R. A., ed.), Ann Arbor Science Publications, Ann Arbor, MI, pp. 555– 606 Levin, L., Blair, N., De Master, D., Plaia, G., Fornes, W., Martin, C. & Thomas, C. 1997 Rapid subduction of organic matter by maldanid polychaetes on the North Carolina slope. Journal of Marine Research 55, 595–611 Loo, L.-O., Jonsson, P. R., Sko¨ ld, M. & Karlsson, O } . 1996 Passive suspension feeding in Amphiura filiformis (Echinodermata: Ophiuroidea): feeding behaviour in flume flow and potential
feeding rate of field populations. Marine Ecology Progress Series 139, 143–155 Molander, A. 1963 Studies on the fauna in the fjords of Bohusla¨ n with reference to the distribution of different associations. Arkiv fo¨ r Zoologi, Serie 2, 15, 1–64 Nash, R. D. M., Chapman, C. J., Atkinson, R. J. A. & Morgan, P. J. 1984 Observations on the burrows and burrowing behaviour of Calocaris macandreae (Crustacea: Decapoda: Thalassinoidea). Journal of Zoology, London 202, 425–439 Nilsson, H. C. & Rosenberg, R. 1997 Benthic habitat quality assessment of an oxygen stressed fjord by surface and sediment profile images. Journal of Marine Systems 11, 249–264 Nilsson, H.C. & Rosenberg, R. 2000 Succession in marine benthic habitats and fauna in response to oxygen deficiency analysed by sediment profile imaging and grab samples. Marine Ecology Progress Series 197, 139–149. Nordberg, K., Lo¨ fstedt, H. & Malmgren, B. 1999 Oceanographic conditions in the deepest parts of the Kattegat, Scandinavia, revealed through recent benthic foraminifera and hydrography. Estuarine Coastal and Shelf Science 49, 557–576 Nowell, A. R. M., Jumars, P. A. & Fauchald, K. 1984 The foraging strategy of a subtidal and deep-sea deposit feeder. Limnology and Oceanography 29, 645–649 Nowell, A. R. M., Jumars, P. A., Shelf, R. F. L. & Southard, J. B. 1989 The effects of sediment transport and deposition on infauna: results obtained in a specially designed flume. In Ecology of Marine Deposit Feeders (Lopez, G., Taghon, G., Levinton, J., eds), Springer-Verlag, New York, pp. 247–268 Pearson, T. H. & Rosenberg, R. 1978 Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology Annual Review 16, 229–311 Pearson, T. H. & Rosenberg, R. 1987 Feast and famine: Structuring factors in marine benthic communities. In The 27th Symposium of The British Ecological Society Aberystwyth 1986 (Gee, J. H. R., Giller, P. S., eds), Blackwell Scientific Publications, Oxford, pp. 373–395 Petersen, C. G. J. 1913 Valuation of the Sea. 2. The animal communities of the sea bottom and their importance for marine zoogeography. Report of the Danish Biology Annual Review 16, 229–311 Rhoads, D. C. & Boyer, L. F. 1982 The effects of marine benthos on physical properties of sediments. A successional perspective. In Animal—Sediment Relations (McCall, P. L. & Tevesz, M. J. S., eds), Plenum Press, New York, pp. 3–52 Rhoads, D. C. & Germano, J. D. 1982 Charecterization of organism-sediment relations using sediment profile imaging: An efficient method of remote ecological monitoring of the seafloor. Marine Ecology Progress Series 8, 115–128 Rhoads, D. C. & Germano, J. D. 1986 Interpreting long-term changes in benthic community structure: a new protocol. Hydrobiologia 142, 291–308 Rodhe, J., Cederlo¨ f, U. & Liljebladh, B. 1998 Generation of baroclinic tides in the Kattegat—observations and modelling. Annales Geophysicae 16, Supplement II, p. C574 (Abstract) Rosenberg, R. 1995 Benthic marine fauna structured by hydrodynamic processes and food availability. Netherlands Journal of Sea Research 34, 303–317 Rosenberg, R. & Diaz, R. J. 1993 Sulfur bacteria (Beggiatoa spp.) mats indicate hypoxic conditions in the inner Stockholm Archipelago. Ambio 22, 32–36 Rosenberg, R., Hellman, B. & Lundberg, A. 1996 Benthic macrofauna community structure in the Norwegian Trench, deep Skagerrak. Journal of Sea Research 35, 181–188 Schaffner, L. 1990 Small-scale organism distributions och patterna of species diversity: evidence for positive interactions in an estuarine benthic community. Marine Ecology Progress Series 61, 107–117 Schaffner, L. C., Jonsson, P., Diaz, R. J., Rosenberg, R. & Gapcynski, P. 1992 Benthic communities and bioturbation history of estuarine and coastal systems: effects of hypoxia and
Benthic faunal quantity and infaunal burrow structures 853 anoxia. In Marine Coastal Eutrophication (Vollenweider, R. A., Marchetti, R. & Viviani, R., eds), Elsevier, Amsterdam, pp. 1001–1016 Sokal, R.R. & Rohlf, F. J. 1981 Biometry: The Principle and Practice of Statistics in Biological Research. W. H. Freeman, San Francisco Svansson, A. 1975 Physical and chemical oceanography of the Skagerrak and the Kattegatt. Fishery Board of Sweden, Report No.1, pp. 1–88 Tarling, G. A., Matthews, J. B. L., Saborowski, R. & Buchholz, F. 1998 Vertical migratory behaviour of the euphausiid, Meganyctiphanes norvegica, and its dispersion in the Kattegat Channel. Hydrobiologia 375/376, 331–341 Thomsen, L., Graf, G., Juterzenka, K. v. & Witte, U. 1995 An in situ experiment to investigate the depletion of seston above an interface feeder field on the continental slope of the western Barents Sea. Marine Ecology Progress Series 123, 295–300 Thorson, G. 1957 Bottom communities (sublittoral or shallow shelf). Geological Society of America Memoir 67 1, 461–534
Ulrich, J. & Eisele, A. 1993 Die Kattegat-Rinne. Erla¨ uterungen zu einer neuen Tiefenkarte. Deutsche HydrographischeZeitschrift 45, 15–29 Valente, R. M., Rhoads, D. C. & Germano, J. D. 1992 Mapping of benthic enrichment patterns in Narragansett Bay, Rhode Island. Estuaries 15, 1–17 Weston, D. P. 1990 Quantitative examination of macrobenthic community changes along an organic enrichment gradient. Marine Ecology Progress Series 61, 233–244 Zajac, R. N. & Whitlatch, R. B. 1982 Responses of estuarine infauna to disturbance. II. Spatal and temporal variation of succession. Marine Ecology Progress Series 10, 15–27 Zajac, R. N., Whitlatch, R. B. & Thrush, S. F. 1998 Recolonization and succession in soft-sediment infaunal communities: the spatial scale of controlling factors. In Recruitment, Colonization and Physical-Chemical Forcing in Marine Biological Systems (Baden, S., Pihl, L., Rosenberg, R., Stro¨ mberg, J.-O., Svane, I. & Tiselius, P., eds), Kluwer Academic Publishers, Dordrecht, pp. 227–240
Depth Correlated Benthic Faunal Quantity and Infaunal Burrow Structures on the Slopes of a Marine Depression R. Rosenberga, H. C. Nilsson, B. Hellman and S. Agrenius Department of Marine Ecology, Go¨teborg University, Kristineberg Marine Research Station, 450 34 Fiskeba¨ckskil, Sweden Received 6 December 1999 and accepted in revised form 19 February 2000 In the northern part of the Kattegat, western Sweden, a series of marine depressions remain since the last glaciation. One of these, the well-oxygenated Alkor Deep, is about 3 km long and 800 m wide and with a depth of 138 m. Random depth-stratified sampling was made along four transects on the slopes including benthic macrofauna (0·1 m2 grab samples) and sediment profile imaging. A significant positive correlation was found between depth and the faunal variables abundance and biomass. Deposit feeders such as Maldane sarsi, Heteromastus filiformis and Abra alba were among the dominants and may have been supported by down-slope advected organic material. In many images, pockets and extensive burrows were seen in the sediment that appeared to be constructed by the crustaceans Calocaris macandreae and Maera loveni. The ecological significance of their irrigation of the sediment is discussed. Due to the faunal activity deep down in the sediments of the slopes, the mean apparent redox potential discontinuity (RPD) was found as deep as between 8·0 and 11·3 cm depth, and RPD was significantly positively correlated with water depth. On the slopes there appears to be a balance between the input of organic material and the capacity of the benthic organisms to assimilate that carbon. 2000 Academic Press Keywords: sediment profile imaging; bioturbation; deposit feeder; Calocaris; Maera; Melinna; Kattegat
Introduction In the classical papers by Petersen (1913), Thorson (1957) and Molander (1963) it was shown that bottom fauna communities could be homogeneous over large areas and that dominant species appeared repeatedly and characterized these communities. A rather uniform pattern in distribution may, however, be interrupted or gradually changed when environmental conditions change. The time and scale at which a disturbance may occur will have an impact on the faunal succession and structure (Zajac & Whitlatch, 1982; Zajac et al., 1998). It has been demonstrated that hydrodynamically enhanced inputs of food to the benthos can change the faunal composition over short distances (Creutzberg et al., 1984) and locally increase the abundance and biomass significantly (Rosenberg, 1995). These two latter studies support the concept of a strong pelagicbenthic coupling (Josefson & Conley, 1997) and the importance of food availability as a major structuring factor of marine benthos (Pearson & Rosenberg, 1987). a
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Pearson and Rosenberg (1978) and Rhoads and Germano (1982) demonstrated that benthic communities respond in a predictable way to changes in organic input and physical disturbance. Their models also suggested that an increased input of organic carbon would result in an increase of deposit-feeding animals relative to suspension feeders. At a moderate input of organic matter, the vertical depth distribution of infauna in the sediment could increase. Josefson (1981), Dauwe et al. (1998) and Weston (1990) found that a faunal activity down to at least 20 cm within the sediment could occur in the Skagerrak, the North Sea and in coastal areas in the Pacific, respectively. The models cited above on infaunal distribution are useful descriptors of benthic community succession in relation to disturbance. For a thorough understanding of functional aspects, information about faunal bioturbation, irrigation, interaction, and their effects on redox conditions and chemical element fluxes and transformations are needed. The Kattegat is a shallow sea with a mean depth of 23 m (Svansson, 1975). However, a deep channel— the Kattegat Channel System—with depths of around 80 to 100 m is an extension southwards of the 2000 Academic Press
844 R. Rosenberg et al.
F 1. The study area. (a) shows the sampling area, the Alkor Deep (Ad), and also the Deep Trench (Dt) and the Norwegian Trench (Nt), (b) is a detailed map of the Alkor Deep with depth contours and sampling transects (solid lines), (c) is a depth profile along the transect from south-east towards north-west.
Norwegian Trench and the Deep Trench in the Skagerrak (Figure 1). The channel system contains some localized, deep depressions, where the environmental conditions for the benthic fauna are suggested to be extraordinary compared with the surrounding bottoms. These depressions were probably formed as a postglacially influenced periglacial melt-water channel about 15 000 to 11 000 years ago (Ulrich & Eisele, 1993). The present study focused on the Alkor Deep, which is about 3 km long, 800 m wide and with a maximum depth of 138 m. Water temperature and salinity deeper than 70 m were recorded at 4 to 6 C and 33·5 to 34·2 (using the Practical Salinity Scale), respectively (Tarling et al., 1998). The surficial sediments in the deeper part of this depression was found to be of recent origin, and the sedimentation rate suggested to be lower than the 3·2 cm yr 1recorded in an adjacent depression, the Littorina Deep (Blanz, 1992). The deepest part of the depression and the slopes are characterized by fine sediments, whereas on the flatter part, at about 40 m, sand may predominate (Nordberg et al., 1999). Blanz (1992) recorded no methane gas in the sediment in the Alkor Deep and suggested that bottom currents keep some of these depressions rather intact. Currents in the deeper part of the Alkor Deep have been recorded to flow mainly along the main north-south axis [Figure 1(b)] and frequently exceed 10 m s 1 (Buchholz et al., 1995). Another interesting observation is that krill (Meganyctiphanes norvegica) occupies a southern refuge in its distribution, towards more brackish water of Baltic origin, in these depressions (Tarling et al., 1998).
The aim of this study was to investigate the benthic faunal composition and their sedimentary habitat on the slopes and deep bottom of the Alkor Deep. We hypothesize that the steep slopes and the presumably associated sediment transport will represent a disturbance to suspension feeders, but instead promote deposit feeders by intermittent deposition and resuspension of organic material. Signs of infaunal activity in the sediment and the apparent redox profile discontinuity were analysed in images obtained by a sediment profile camera (e.g. Rhoads & Germano, 1986). The same methods were used in a nearby area, the Deep Trench (Figure 1), where bottom-near currents mediated a horizontal transport of food particles and where an extremely high sedimentation rate occurred on one side of the slope (Rosenberg, 1995). In the present study we show that the faunal abundance and biomass and redox conditions on the slopes of the Alkor Deep increased with depth. This is part of a joint research project where Nordberg et al. (1999) have analysed foraminiferans in relation to hydrographic conditions and Rodhe et al. (1998) studied current regimes. Material and methods Sampling was carried out on 19 to 22 September 1994. Sediment profile images (SPIs) and grab samples of infauna were randomized in 20 m depth intervals from the slopes down to the deepest part of the Alkor Deep (Figure 1). Within these depth strata, the sample sites were distributed around four transects
Benthic faunal quantity and infaunal burrow structures 845
800
(a)
60
(b)
2
R2 = 0.34 Biomass (g 0.1 m–2)
Abundance (0.1 m2)
R = 0.53 600
400
200
0 16
50 40 30 20 10 0
(c)
(d) 2
R = 0.46
13
R2 = 0.33
BHQ-index
RPD (cm)
12
8
4
0 40
11 9 7
60
80 100 Depth (m)
120
140
5 40
60
80 100 Depth (m)
120
140
F 2. Linear positive correlations with depth and abundance (a), biomass (b), apparent Redox Profile Discontinuity (RPD) (c), and Benthic Habitat Quality (BHQ) index (d) in the Alkor Deep.
and numbered according to compass directions from Alkor Deep, NE (25), SE (135), SW (205) and NW (315) [Figure 1(b)]. The depth strata were 80–99, 100–119 and 120–138 m for all four transects. In the NW and SE directions the bottom levelled off at 40 m and here also the depth strata 40–59 and 60–79 were sampled. The samples in the different strata were named after transect directions and shallowest depth of stratum, e.g. NW40, NW60, etc, and the deepest stratum is named A120. Four in situ Sediment Profile Images (SPIs) were taken in each stratum, except in stratum NE80 where the camera failed. Images were taken through a prism (30 cm long, 22 cm wide; see Rosenberg & Diaz, 1993). The contrast of the colour of the sediment was digitally enhanced in Adobe Photoshop 4.0. Depth of mean apparent Redox Potential Discontinuity (RPD; Fenchel & Riedel, 1970) was analysed in NIH image 1·6. The Benthic Habitat Quality (BHQ) index was calculated in each image, where (a) the sediment surface and (b) sub-surface structures and (c) the apparent RPD were parameterized. The BHQ index range between 0 and 15, where low indices indicate poor faunal conditions in the sediment and values >10 stands for later stage seral communities (Nilsson & Rosenberg, 1997, 2000).
Infauna was collected by taking four samples in each stratum with a 0·1 m2 Smith-McIntyre grab, totally 56 samples. The grab was filled with sediment at all occasions and penetrated to a maximum depth of 18 cm. The sediment was sieved through a 1 mm mesh and the fauna was picked out gently and preserved in 70% ethanol. Infaunal similarity was analysed by applying the Bray-Curtis similarity coefficient to √√-transformed abundance and biomass data of all taxa; based on this index the samples were analysed by MultiDimensional Scaling (MDS; Clark & Warwick, 1994). Correlations between sampling depth and fauna and sediment parameters were analysed by simple linear regression. Statistical significance of regressions was tested by Kendall’s rank correlation coefficient (Sokal & Rohlf, 1981). Results Faunal composition and quantity A significantly positive correlation (R2 =0·53, P<0·001) was found between depth and mean total abundance of fauna [Figure 2(a)]. At depth strata between 40 and 79 m, mean abundance per 0·1 m2
846 R. Rosenberg et al.
was <200, and in the deepest strata abundance was >400 (Table 1). Similarly, a significant positive correlation (R2 =0·34, P<0·001) was found between depth and mean biomass [Figure 2(b)]. In the depth strata 40 to 79 m, mean biomass per 0·1 m2 was 5·8 to 19·2 g wet weight and in all deeper strata it was higher, between 19·9 and 37·1 g. Mean number of taxa per 0·1 m2 in the area was between 24 and 38 with no depth correlation. Total number of taxa was 150. Significantly negative correlations between Shannon-Wiener diversity H (R2 =0·49, P<0·001) and evenness J (R2 =0·53, P<0·001) and depth were recorded. Most of the three dominant species in each depth strata were present over the whole area but with highest numbers at greater depths (Table 1). The tube-building polychaete Maldane sarsi had high abundances in several of the deep strata, but was almost absent along the SE-transect. The head-down deposit-feeding polychaete Heteromastus filiformis was found in highest numbers on the slopes. The surface deposit-feeding bivalve Abra nitida had a rather homogeneous distribution over the whole area varying in numbers between 13 and 84 per 0·1 m2. Most of the species in the area were surface or sub-surface deposit feeders. If the brittlestar Amphiura filiformis, which can be both a suspension feeder and a deposit feeder (Loo et al., 1996), was excluded from a comparison of feeding groups in the Alkor Deep, about 90% of the individuals would be classified as deposit feeders, about 10% as predators and almost no suspension feeders. Most of the deposit feeders were feeding on the sediment surface. The crustaceans Maera loveni and Calocaris macandreae are known to dig extensive burrows in muddy sediment (Atkinson et al., 1982; Nash et al., 1984). They were present in most samples (Table 1). The small epifaunal brittlestar Ophiura affinis occurred in numbers between 5 and 27 per 0·1 m2 at depths greater than 100 m. Several individuals of the peculiar ‘ mast ’ building crustacean Dyopedos monacanthus were found in the deep strata A120 and NW100. The hagfish Myxine glutinosa was captured in several grabs from depths below 80 m, but was excluded from this presentation. Dominants in biomass were the heart urchin Brissopsis lyrifera (0–11·5 g wet wt per 0·1 m2) and the brittlestars Amphiura chiajei (0·3–4·8 g) and A. filiformis (0-8·6 g). Multivariate analyses of abundance and biomass showed similarities within the strata SE40, NW40 and SE60; for abundance also for NW60 and SE80 (Figure 3). The deeper strata d80 m generally grouped together and were separate from the shallow strata. Thus, a difference in faunal composition was found
between the shallow stations and for those on the slopes and bottom. Sediment and sediment profile images The organic carbon content in the upper 2 cm of the sediment in the Alkor Deep varied between 2·1 and 2·5% of the dry weight (Table 1; data from Nordberg et al., 1999). Mean penetration of the prism into the sediment was between 10·6 and 20·7 cm (Table 1), and increased significantly with depth (R2 =0·23, P<0·01) indicating softer sediments in deeper water. Burrow structures and voids were seen in almost all images and infauna in about half of them. In many images, oxic voids were found deeper than 10 cm in the sediment with a mean maximum depth of 18·8 cm, indicative of deep feeding and irrigation activity. Depth of mean apparent RPD was, with one exception, >3 cm and in some strata >10 cm. Apparent RPD was significantly positively correlated with depth [R2 =0·46, P<0·001; Figure 2(c)]. These observations are clear indications of an extensive faunal activity deep within the sediment. Activity of infauna was seen in all images from the Alkor Deep. Six SPIs are presented from different depths (Figure 4). The rust-brown colour is indicative of the oxidized sub-oxic zone. The sediment is reworked in the upper centimetres. The large burrows and tunnels observed in the images from 60 m and deeper were probably made by Calocaris macandreae and Maera loveni. The image A120 shows two large burrows extending down towards the bottom of the picture, which seem to lead even further down in the sediment. An arm of a brittlestar is seen in the middle of the left burrow. In image NE100 several polychaetes are visible that are suggested to be head-down feeding Heteromastus filiformis. Similarly, in image SW80, SE80 and SE60 extensive burrow systems are visible, and also indications of vertical burrows or tubes that in some cases extend all the way to the bottom of the images. Some of these are suggested to indicate the presence of Melinna cristata, H. filiformis and Maldane sarsi. In the SE44 image the sediment surface is uneven with sand at the top and clay below. The surface is reworked and the pockets could be made of Abra nitida or Amphiura filiformis. Only few tubes and no other structures are seen above the sediment surface. Mean BHQ indices varied between 8·0 and 11·3, and a significant positive correlation (R2 =0·33, P<0·001) was found with depth [Figure 2(d)]. At depths below 80 m, individual images always had BHQ indices d9, and the mean indices in each of these deeper strata were >10. This is indicative of an
a
From Nordberg et al. (1999).
Dominant species Maldane sarsi Heteromastus filiformis Abra nitida Amphiura filiformis Amphiura chiajei Leucon nasica Spiophanes kroeyeri Chaetozone setosa Alvania testae Deep burrowing species Maera loveni Calocaris macandreae Community variables Mean total abundance Mean total biomass Mean no. of taxa Diversity H Evenness J Sediment measurements Mean penetration Mean RPD Mean BHQ Max depth of tunnel or void Organic carbon (%)a
Average depth (m)
2 + 1 412 28·3 27 2·3 0·7 16·0 9·3 11·5 15·3 2·4
3 1 449 31·6 33 2·4 0·7 20·2 10·2 10·7 18·8 2·5
99 66 78 34 22 36
NE 100 107
81 72 80 49 25 29 6 3
A 120 126
20·0 10·8 10·8 17·0 2·4
463 37·1 32 2·4 0·7
2 +
75 70 80 73 14 27 7 4
SW 100 113
20·7 12·0 11·0 16·2 2·3
456 28·3 35 2·4 0·7
2 1
113 64 80 45 15 11 9 3
NW 100 112
13·9 7·9 11·0 12·7 2·3
584 29·4 34 1·9 0·5
1 +
311 49 76 9 15 10 1
SE 100 110
2·3
258 24·6 28 2·4 0·7
+ 2
1 88 31 30 10 20 6 3
NE 80 88
19·1 9·6 11·0 14·0 2·3
335 27·5 30 2·3 0·7
1
105 69 36 8 17 17 9
SW 80 92
18·5 5·9 11·3 16·8
529 33·4 34 2·4 0·7
1 1
124 77 84 65 14 11 6 4 +
NW 80 98
12·7 3·6 10·8 8·9 2·3
204 19·9 29 2·4 0·7
1 1
+ 29 61 35 7 5 12 4
SE 80 91
14·0 4·1 7·0 12·8
147 19·2 30 2·7 0·8
1 1
2 23 26 3 12 8 12 4 2
NW 60 76
17·8 6·6 9·3 12·2 2·4
117 7·6 24 2·5 0·8
+
+ 34 13 3 5 11 8 7
SE 60 75
13·2 3·0 9·3 7·4
196 17·1 37 2·9 0·8
+
1 25 32 10 20 8 2 2 5
NW 40 46
10·6 2·6 8·0 8·4 2·1
159 5·8 38 3·1 0·9
1
+ 2 35 6 1 1 5 11 12
SE 40 51
T 1. Alkor Deep. Mean benthic faunal (per 0·1 m2) and sediment data at the different depth strata; (a) abundance of the 3 dominant species at each station, and (b) of deep burrowing crustaceans, (c) community variables, and (d) measurements of sediment profile imaging. +indicates single occurrence
Benthic faunal quantity and infaunal burrow structures 847
848 R. Rosenberg et al. Abundance
Stress = 0.20
Biomass
Stress = 0.20
NW40
NW40
SE40 SE40 SE60
NW60 SE80 SE80
SE60
F 3. Plots showing the faunal similarities as Multi-Dimensional Scaling (MDS) based on abundance (left) and biomass (right) data. Some depth strata that group together are encircled.
equilibrium successional stage III benthic community (Nilsson & Rosenberg, 1997). Discussion Benthic community distribution The community structure of the benthic fauna in the Alkor Deep is related to depth. In each of the two shallow depth strata at 40 to 59 and 60 to 79 m, the faunal compositions were rather uniform (Figure 3). One reason for the differences in community structure could be that at depths of 46 to 67 m patches of sand occurred (Nordberg et al., 1999), which could have affected the faunal composition. In addition, larger areas were sampled at the shallower depths compared to on the slopes with a possible greater variation between samples as shown in the MDS-plot. All deeper stations grouped together in the MDS-plot, and the faunal structure was separated from those above 80 m depth. Distribution of foraminiferans was investigated during the same survey as the present (Nordberg et al., 1999). The authors of that study concluded that the species composition of foraminiferans showed a discontinuity in distribution at about 80 m water depth. They attributed this to similarities in deep-water hydrography, and they concluded that the Alkor Deep does not have stagnant water but is connected to the deeper areas further north. In the present study, the benthos on the slopes and in the deepest part had higher abundance and biomass
compared with the shallower and flatter area. We suggest that these gradual increases in faunal quantity on the slopes are mainly due to differences in bottom current mediated down-slope transport of organic particles. Availability of food in surplus for the benthos has been shown in this sea area to enhance faunal numbers and biomass (Josefson & Jensen, 1992; Rosenberg, 1995). Deposit feeding and particle transport Approximately 90% of the animals on the slopes of Alkor Deep feed on the particles deposited on, or in, the sediment. Little is known about the ecological effects of sediment transport and deposition rates on deposit-feeding animals (Nowell et al., 1989). It has been demonstrated that near-bottom currents are important for lateral particle flux and for the supply of food for benthic animals (Thomsen et al., 1995). Resuspension of particles is determined by water flow rate, bottom shear velocity and bottom roughness (Jumars, 1993; Graf & Rosenberg, 1997). Benthic animals can either stabilize or destabilize sediments and thus have a direct impact on the erodibility (Rhoads & Boyer, 1982; Jumars & Nowell, 1984). It has been demonstrated that spionid polychaetes respond positively to moderate sediment transport by increased feeding and fecal pellet production (Dauer et al., 1981; Nowell et al., 1989). Some species that are sub-surface feeding may also be able to collect food particles on the surface (Levin et al., 1997) and
Benthic faunal quantity and infaunal burrow structures 849
F 4. Sediment profile images from the strata A120, NE100, SW80, SE80, SE60 and SE40. The contrasts are enhanced to better visualize burrows, voids and the Redox Potential Discontinuity (RPD). The rust-brown colour indicates the oxidized sub-oxic zone. Burrow structures that appear to be constructed by Calocaris macandreae and Maera loveni are clearly seen in the images from 60 m and deeper. Several polychaetes, probably Heteromastus filiformis, are seen in the NE100 image. The vertical scale is centimetres, and the black rectangle masks reflections of the flash.
may take advantage of this when particles transported down-slope can be captured. Other deposit feeders may be dependent on the rate of sedimentation into their feeding depressions (Nowell et al., 1984). Graf and Rosenberg (1997) showed that biodeposition of particles on the sediment surface are of significant quantitative importance. The above information about deposit feeders demonstrates that some species are able to adjust to variations in sediment transport and that this transport can provide an additional food supply. Thus, the increases in numbers and biomass of the infauna on the slopes of the Alkor Deep are suggested to be a response to down-slope transport of sediment-associated food particles.
The impact of infaunal bioturbation and biodeposition on resuspension has been documented, especially for deposit feeders, e.g. by Davis (1993) and Graf and Rosenberg (1997). Deposit feeding accounts for most bioturbation of particles in the sediment because deposit feeders feed at a high rate and use separate sites of ingestion and egestion (Jumars & Wheatcroft, 1989). The sediment surface observed in the SPIs always showed signs of infaunal activity, and large-scale erosions seem not to occur on the slopes or deep bottoms in this area. The disturbance caused by the activity of the deposit feeders may, together with down-slope sediment transport, create a physical disturbance unsuitable for
850 R. Rosenberg et al.
suspension feeders and even some deposit feeders. For example, Hollertz et al. (1998) have shown that activity of Brissopsis lyrifera can negatively affect the growth of Amphiura chiajei. Moreover, active burrowing crustaceans my destabilise the sediment when feeding and moving, which is likely to have a negative impact on some sessile and stationary animals such as tube builders (Brenchley, 1981). Comparisons of faunal distribution In the deepest part of the Norwegian Trench in the Skagerrak [Figure 1(a)], the composition of the macrofauna showed a discontinuity at about 400 m (Rosenberg et al., 1996). Josefson (1985) found major divisions in faunal community distribution between the depth intervals 40–200, 200–360 and 360–650 m in the eastern Skagerrak. Comparisons showed that abundance was lower, and biomass much lower, both on the slopes and in the deep part of the Norwegian Trench compared with the Alkor Deep slopes. The organic content in the surface sediments were similar in both areas, but due to the difference in water depth, the carbon was probably more refractory in the Norwegian Trench. The benthic fauna in the Deep Trench in the south-east Skagerrak [Figure 1(a)] was studied by Rosenberg (1995). Both the western slopes and the deeper bottoms at 100 m of this trench had a macrofauna abundance that was higher, or much higher, at all stations (up to 13 600 ind m 2). Also the biomass was higher in the Deep Trench than in Alkor Deep on several stations, and so was the organic content in the surficial sediment (2·8 to 3·4%). The author explained the extremely high abundance and generally high biomass in the Deep Trench to be caused by a great transport of organic particles in the bottom-near water, and an extremely high sedimentation rate. It was suggested that the animals were not limited by food but rather by space. Thus, hydrodynamic processes most probably advected food particles that optimised the conditions for the benthic fauna. Faunal activity deep in the sediment The SPI complements the information about the sedimentary habitat that is usually obtained by taking grab samples and analysing the fauna. SPIs give an in situ view of the sediment redox conditions and faunal activity (Rhoads & Germano, 1986). Parameterization of the information has proven to be useful, and the Benthic Habitat Quality (BHQ) index is related to the successional stages in the Pearson-
Rosenberg (1978) model (Nilsson & Rosenberg, 1997, 2000). The BHQ indices were >10 on the slopes and are indicative of late successional stage communities. Thus, these types of benthic communities have most probably been present in the area for decades, which suggests, in agreement with Nordberg et al. (1999), that the bottoms of the Alkor Deep are well flushed. In 1995, the total organic content in the surficial sediment along the Swedish Skagerrak coast was found to be between 0·9 and 3·7% of the dry weight with a mean of 2·5% (Cato, 1997). In comparison with that mean and percentages given above for the Norwegian Trench and the Deep Trench, the sediments on the slopes in Alkor Deep (Table 1) seem not to have an enhanced content of carbon. The mean of the apparent RPD is very high in comparison with other similar studies in coastal areas on the U.S. east coast (Grizzle & Penniman, 1991; Schaffner et al., 1992; Valente et al., 1992), the Baltic (Bonsdorff et al., 1996), and the Deep Trench (Rosenberg, 1995), the Norwegian Trench (Rosenberg et al., 1996) and fjords in the Skagerrak (Nilsson & Rosenberg, 1997, 2000). This deep apparent RPD is a consequence of faunal activity down to great depths in the sediment, and suggests that the organic carbon is not accumulated but rather assimilated. It is likely that the deep-burrowing species Calocaris macandreae and Maera loveni contribute to the oxygenation of the sediment and the mineralization of carbon (Forster & Graf, 1992). Many species are likely to live in close contact with the burrows constructed by these species (Dauwe et al., 1998) and contribute to the breakdown of organic material. Several individuals could be in the meiofaunal size range, which were not included in this study. The mean depth of the apparent RPD in the Deep Trench was much lower (<5 cm) than in the Alkor Deep. This in combination with the comparatively higher organic content in the sediment implies that the transport of organic material to the bottoms in the Deep Trench was higher than in the Alkor Deep or took longer to mineralize. Deep burrowing crustaceans like C. macandreae and M. loveni and the rather large tube-building polychaete Melinna cristata were missing in areas with high organic deposition in the Deep Trench. The comparatively lower abundance of A. filiformis and the associated small bivalve Mysella bidentata in the Alkor Deep compared with the Deep Trench could be caused by interspecific disturbance of these tunnel-building crustaceans, or that the amount of horizontally advected food was less. In summary, we conclude that in the Alkor Deep there appears to be a balance between input of organic material and the capacity of the benthic organisms to
Benthic faunal quantity and infaunal burrow structures 851
assimilate that carbon. This balance seems to have persisted for a long time, probably decades, as the benthic fauna was assessed to be in an equilibrium successional stage. The maximum depth where tunnels and voids were seen in the SPIs were 18·8 cm and in most cases below 10 cm in the sediment. In some samples signs of faunal activity was close to the depth of mean penetration of the prism. Thus, these large burrow structures were common over the whole area and most pronounced on the slopes. Dauwe et al. (1998) showed that infauna occurred down to about 20 cm in the sediment at three stations in the North Sea and the Skagerrak. They also recorded the largest individual sizes and the deepest distribution where the organic matter was of intermediate quality and quantity. Estimates of tunnel areas and volumes in the sediment The bioturbation and biodeposition in the Alkor Deep was not measured, but it is probably significant (see below) and important for the rate of mineralization. It appears from the grab samples that the deep, large burrow structures observed in the SPIs are made by the mud shrimp Calocaris macandreae and the amphipod Maera loveni (Table 1). Their burrowing activity and tunnel constructions are described in papers by Atkinson et al. (1982) and Nash et al. (1984) and some details from those publications are summarized below. Both species spend almost all time in their burrows. These are initially U-shaped and later elaborated with vertical tunnels and further openings to the surface. The tunnels of C. macandreae descend deep down into the sediment and frequently form a second level of horizontal tunnels. The tunnel diameter has been measured at 14 to 19 mm for C. macandreae, and on average 19 mm for M. loveni. The maximum depths for both species can in some cases extend vertically beyond 20 cm. Thus, it seems not possible to separate the burrow systems into species in the SPIs. The variations in sediment tunnel area and volume in burrows of C. macandreae and M. loveni were found to be large, but crude averages of tunnel areas occupied by single individuals could be 0·1 and 0·05 m2, with volumes corresponding to 0·5 and 0·1 l, respectively (Atkinson et al., 1982; Nash et al., 1984). At depths below 80 m in the Alkor Deep every square metre may be occupied by 10 C. macandreae and 10 M. loveni (Table 1). With such assumptions, the two crustaceans can have tunnels in the order of 1·5 m2 with a volume of 6 l per m2. Tunnels and voids were seen in most of the SPIs from below 60 m water depth. These descended to depths below 12 cm, and
as these structures frequently were large, they were probably tunnels made by C. macandreae and M. loveni. Their irrigation of at least parts of the tunnel system will be beneficial for other infaunal organisms (Schaffner, 1990) and have significant effects on the geochemistry in the sediment (Gilbert et al., 1998). The bioturbation rates of these animals have not been assessed, but records from other areas suggest that it can be high for many species (Lee & Swartz, 1980; Diaz & Schaffner, 1990). The two crustaceans were collected in most of the grab samples, but their abundances were most likely underestimated as the grab only was biting down to a maximum depth of 18 cm and animals deeper down or on the outside of each half of the grab were not collected. It seems therefore that the bottoms of the Alkor Deep are extensively bioturbated, especially below about 80 m water depth.
Acknowledgements We thank the crew on RV Skagerak and Dr Mattias Sko¨ ld for technical assistance; Dr Kjell Nordberg for comments of the manuscript; and the Swedish Natural Science Research Council and the Go¨ teborg University Marine Research Centre for financial support.
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