Deep-sea macrofaunal impacts of a large-scale physical disturbance experiment in the Southeast Pacific

Deep-Sea Research II 45 (1998) 55—81

Deep-sea macrofaunal impacts of a large-scale physical disturbance experiment in the Southeast Pacific Christian Borowski*, Hjalmar Thiel Alfred-Wegener-Institute for Polar and Marine Research, Columbusstr., 27568 Bremerhaven, Germany Received 15 February 1997; received in revised form 10 September 1997; accepted 20 September 1997

Abstract Future human use of the deep sea potentially threatens benthic communities on large spatial and temporal scales. As a first approach to investigating the effects of large-scale sediment disturbance from deep-sea mining, the environmental risk assessment experiment DISCOL (DISturbance and ReCO¸onization) was started in 1989 at 4150 m depth in the tropical southeastern Pacific Ocean. A specially constructed disturber was towed 78 times through a 10.8 km2 experimental field. The reestablishment of the impacted macrofaunal assemblages in the disturber tracks, with particular emphasis on the Polychaeta, was monitored three times over 3 yr. Mean macrofaunal densities ('500 lm, 0—5 cm sediment depth range) in undisturbed sediments ranged from 77 to 122.8 inds./0.25 m2 at the three sampling times. After the impact, the animal abundances in the plow tracks were reduced to 39% of undisturbed densities. Polychaeta (48.6% of undisturbed densities) were less impacted than Tanaidacea (28.0%), Isopoda (18.5%), and Bivalvia (9.3%). Abundances of most higher taxa increased rapidly in the tracks, and after 3 yr were comparable to those of undisturbed sediments. Dominance shifts in polychaete families level were observed in the early post-impact phases. Significant displacement of macrofaunal depth distributions after 3 yr indicated sustained disturbance effects. Single species reactions within the Polychaeta did not allow clear interpretation of long-term disturbance effects, but Hurlbert rarefaction, used in a nonstandard way, demonstrated significantly reduced “diversity” after 3 yr. The reestablishment of a semi-liquid surface sediment layer is proposed as a potentially controlling factor for the reestablishment of the macrofaunal community after physical disturbance. Although the DISCOL experiment did not fully simulate full-scale industrial impacts, it has provided insights into macrofaunal recolonization following large-scale disturbance of deep-sea environments. ( 1998 Elsevier Science Ltd. All rights reserved.

* Corresponding author. 0967-0645/98/$19.00 ( 1998 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 9 7 ) 0 0 0 7 3 - 8

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Keywords: DISCOL experiment; Physical disturbance; Manganese nodule mining; Deep-sea macrofauna; Polychaeta; Recolonization; Deep-sea risk assessment

1. Introduction A longstanding issue in deep-sea ecology is whether benthic communities possess the potential to recolonize heavily disturbed areas. Disturbances of biogenic origin that influence the diversity of habitats and organisms generally have limited spatial dimensions from tens of square centimeters to a few square meters (Dayton and Hessler, 1972; Stockton and DeLaca, 1982; Smith, 1986; Smith et al., 1986; Grassle and Morse-Porteous, 1987). Future industrial activities in the deep sea will cause large-scale disturbances of benthic communities. Severe impacts can be expected from deep-sea mining (Jumars, 1981) or large-scale waste disposal, and the recovery of communities after these disturbances is hypothesized to take several years to decades (Thiel, 1992a). A number of in situ disturbance experiments have introduced defaunated sediments into the deep sea (Grassle, 1977; Desbruye`res et al., 1980, 1985; Levin and Smith, 1984; Grassle and Morse-Porteous, 1987; Kukert, 1991; Kukert and Smith, 1992; Snelgrove et al., 1992, 1994). Because of the artificial setups and the necessarily small size of these experiments, it has been difficult to deduce the potential effects of large-scale impacts from anthropogenic use of the deep sea. Environmental studies have been conducted in connection with prepilot mining tests (PPMT) MESEDA (MEtalliferous SEDiment Atlantis II) in the Red Sea and DOMES (Deep Ocean Mining Environmental Study) in the Pacific, but these studies were based on an oceanographic research scale and are similarly difficult to extrapolate to full industrial mining (Jumars, 1981; Karbe, 1987; Thiel, 1991). The PPMTs indicated that long-term monitoring of large-scale disturbed areas is required for realistic risk assessment of deep-sea mining. Two types of large-scale mining impact experiments have been implemented: During the Benthic Impact Experiments (BIE) of the National Oceanic and Atmospheric Administration (NOAA), the Mineral Mining Agency of Japan (MMAJ; Fukushima, 1995), and the Interoceanmetal Joint Organization (IOM), autochthonous sediments were discharged several meters above the seabed to investigate the potential impact of a redepositing sediment plume that will be generated by manganese nodule mining. The German DISturbance and reCO¸onization experiment (acronym: DISCOL) was the first attempt to simulate the effects of large scale sediment disturbance on the deep-sea bottom, such as would be expected from industrial activities in the deep sea, like manganese nodule mining. The goal of DISCOL was to determine the long-term effects of a severe disturbance on community structure by monitoring the reaction of “indicator taxa”, a selection of taxa which we believed would indicate changes best (Thiel, 1992b). Bluhm et al. (1995) described the resultant disturbance effects on the megabenthos. We report in this paper the response of the sediment dwelling macrofauna, with particular emphasis on the dominant Polychaeta, to the DISCOL experiment during the 3 yr following the disturbance.

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2. Study site, experimental setup, materials and methods 2.1. The study site The DISCOL experiment was conducted in a manganese nodule field in the abyssal Peru Basin (southeast equatorial Pacific) (Fig. 1). We chose an obstacle-free plain with moderate nodule population that allowed good operation of the disturber. The DISCOL Experimental Area (DEA) was a circular experimental field with a diameter of 3.6 km, covering approximately 10.8 km2 (Foell et al., 1990, 1992; Thiel and Schriever, 1990). The water depths at the sample sites ranged from 4122 to 4201 m. The hydrodynamic near-bed regime (15 m above bottom) was dominated by slow, alternating directed currents of 3—4 cm/s; peak velocities of '10 cm/s occurred irregularly for short periods of a few hours. The maximum current speed observed during a period of 861 days between September 1989 and January 1992 was 14.7 cm/s (integrated over a measured interval of 3 h; Klein, 1993). Bottom water temperature was 1.5°C. Undisturbed sediment surfaces were more or less smooth, consisting of fine-grained, dark brown, silicate oozes (Fig. 2A). Roughly, the top 2 cm consisted of very smooth, semi-liquid material, while the sediments in deeper layers were progressively consolidated until they changed below 7—10 cm into lighter colored, adhesive clay with high contents of biogenic carbonate. The percent cover of the botryoidal manganese

Fig. 1. Location of the DISCOL Experimental Area in the southeast tropical Pacific Ocean.

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nodules (cf. Halbach and Puteanus, 1988) in the DEA maximally reached 45%, but usually was 5—15%. 2.2. The DISCOL experiment Between 21 February and 16 March 1989, the German R. V. Sonne towed a specially constructed 8-m wide “plow-harrow” that resembled a farmer’s plow (Thiel and Schriever, 1990: Fig. 10) 78 times through the circular experimental field on the deep-sea floor. The plow shares penetrated 10—15 cm deep into the sediments. The resultant tracks (8 m wide by 10—15 cm deep), covered approximately 20% of the DEA and were recognizable in video observations and grab samples even after several years. Video and photo surveys showed that large areas in the DEA were blanketed with redeposited sediments (Thiel and Schriever, 1990; Bluhm et al., 1995). The recolonization of the disturbed areas by meio-, macro-, and megafauna was investigated over the subsequent 3 yr. For detailed descriptions of the experimental design of DISCOL, see Thiel and Schriever (1990) and Foell et al. (1990, 1992). After experimental treatment, the surface sediments in the tracks resembled broken up plow tracks on a farmer’s field. In video observations of the DEA, we recognized heavily disturbed areas with high track densities, alternating with lower impacted areas and undisturbed regions. The semi-liquid sediment was nearly eliminated in the tracks, where surfaces were covered with sharp-edged sediment blocks and lighter colored clay plowed up from deeper layers. Manganese nodules were plowed under (Fig. 2). Six months later, the appearance of the disturbed areas ranged from still stable plow-harrow tracks without semi-liquid sediments to areas with high smallscale surface variability: The semi-liquid layer had begun to reestablish, and depressions between the sediment blocks were refilled with soft material to varying extents. Three years after impact, many tracks were filled, and their surfaces displayed more or less smoothened contours (Fig. 2). Clay sediments, originating from deeper layers, were still recognized at the surfaces as smoothened, light colored patches. 2.3. Sampling and processing Box-core samples (0.25 m2, cf. Fleeger et al., 1988) were collected during three cruises with the German R.V. Sonne in February and March 1989 (cruise name DISCOL 1), in September 1989 (DISCOL 2), and in February 1992 (DISCOL 3). Because the disturber tracks were directed radially through the DEA, we expected the heaviest impacts in the central parts of the experimental field and concentrated our sampling in two target areas: an inner circle and a peripheral ring, separated by a ring-shaped buffer zone (Fig. 3). We divided the DEA into eight sectors and randomly chose five independent sampling sectors in each of the two target areas. The ship positions at the sites were controlled with TRANSIT SATELLITE NAVIGATION and GLOBAL POSITIONING SYSTEM (GPS). The initial plan was to sample three replicates in each of the ten sampling sectors at each sampling time: pre-impact and post-impact (DISCOL 1/1 and DISCOL 1/2), and at all later expeditions. Although pre-impact samples were collected, we could not

Fig. 2. In situ photographs of sample sites made during the sampling procedure with a single shot camera, mounted on the box corer’s frame. A weight at the end of a 1.5 m long cord triggered the camera before the touch-down of the corer. The area in the photograph corresponds to approximately 0.8]1.2 m seabed. (A) Undisturbed sediment before plowing, with manganese nodules, Xenophyophores and various animal traces. (B) Disturbed sediment in March 1989, one week after we finished the plowing. Sharp edged blocks of carbonate-rich clay filled the tracks. Manganese nodules were plowed under. (C) Three years after the impact, many tracks were refilled with soft material. Light colored patches signified that carbonate-rich clay from deeper layers was still exposed.

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.

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Fig. 3. Sample sites within and outside of the DEA (reference locations) during the expeditions: L"DISCOL 1 (post-impact), *"DISCOL 2, and j"DISCOL 3. The southern reference site at approx. 5.9 km south of the DEA center was sampled during DISCOL 2 and DISCOL 3. The locations of the plow-harrow tows (inset) are extrapolated from ship positions during plowing.

compare these to the post-impact collections because the sampling methods had to be altered repeatedly between expeditions as well as between the pre-impact and postimpact phases of DISCOL 1. Since it was not clear whether the observed significant abundance differences between pre-impact and post-impact samples were due to the impact or to the use of different sampling methods, we excluded pre-impact samples from our analyses, and all DISCOL 1 data presented in this paper refer to the post-impact situation. Two types of post-impact samples were identified: (1) Samples obtained from the plow tracks showed clear evidence of the impact (e.g. uneven surface; lack of the semi-liquid top layer; exposed lighter colored sediment originating from deeper layers). Apparently, depending on whether a sample was positioned in the center or more to the edge of a plow-harrow track, these disturbed characteristics were displayed to varying extents. (2) In samples from the areas between the tracks, the entire top sediment layer was smooth and semi-liquid. While the tracks were more or less obvious, we could not identify the thin layers of the resedimented plume in the between-track samples. Since we could not use pre-impact samples to assess the plume impact, we made comparisons between post-impact samples that may have been affected with different intensities. Assuming that the central circle of the DEA was more impacted than the peripheral ring, we tested the mean macrofaunal abundances ('500 lm, 0—5 cm sediment depth) of between-track central samples against those of the peripheral ones (in case of homogeneity of variances and normal distributions we used the double sided t-test, otherwise the nonparametric Whitney—Mann U-test). Twenty-three tests were performed separately for the total macrofauna and 22 higher

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macrofaunal taxa from DISCOL 1 (post-impact) at different levels of orders to phyla. Similar tests were done separately for DISCOL 2 and DISCOL 3. The following sample-type terminology is used throughout this study: Samples with clear track characteristics on at least parts of their surfaces are categorized as “disturbed”, whereas those from the between-track areas are assigned to the “undisturbed” group. The decision whether a sample was disturbed or undisturbed was made on ship board after careful inspection of the surface sediment. In DISCOL 1 and DISCOL 3, the interpretation of the surface structures was supported by comparison with in situ photographs of the sea bed, taken with Preussag FBK 135 cameras during the sampling procedure (Fig. 2). Samples that did not allow clear categorization because they displayed artifacts that possibly were created during the sampling procedure (e.g. uneven sediment surfaces without any white clay) were excluded when the respective in situ photograph did not confirm that the sample site was a plow track. The in situ cameras were not available in DISCOL 2. For this expedition, some uncertainty remains for the correct classification of certain disturbed samples. In two disturbed DISCOL 2 samples, the semi-liquid surface was completely absent and the contours of the plow harrow were still recognizable; these are described as “track” samples. During DISCOL 2 and DISCOL 3, we additionally sampled uninfluenced reference sites outside of the DEA (“reference” samples). Their appearances resembled those of the undisturbed category. As near-bottom currents during the plowing in February/March 1989 were predominantly directed to the north, we chose three reference sites to the west, south, and southeast of the DEA, with distances to the center of the DEA of some 5—7 km. These sites were far enough from the nearest tracks to be uninfluenced by the plowing (Fig. 3). Due to unsuccessful box-corer deployments at some reference stations in DISCOL 2, six of nine reference samples from this expedition were obtained from the southern site. In DISCOL 3 we concentrated on the southern reference location. The total numbers of analyzed samples from DISCOL 1 (post-impact) are: seven disturbed and 21 undisturbed samples; from DISCOL 2: eight disturbed, 22 undisturbed, and nine reference samples; from DISCOL 3: nine disturbed, 20 undisturbed, and eight reference samples. Manganese nodules were carefully removed from the samples, and the sediments were washed over sieves of various mesh sizes to extract the fauna. During DISCOL 1, 1000 lm meshes were used for the entire sample surfaces, but only one 25]25 cm subsample per box-core sample was processed with 500 lm meshes. As this procedure raised the standard deviations and also turned out to be inadequate for quantitative species analysis, we processed the whole sample surfaces at 500 lm in DISCOL 2. During DISCOL 3, we used 250 lm sieves and later split the preserved samples into size fractions. A comparison between results from different size fractions from 13 DISCOL 3 samples revealed that the '500 lm fraction included 59.1% of all macrofauna retained on the 250 lm sieves, and 63.5% of all macrofauna included in all '300 lm fractions (Polychaeta: 61.5 and 65.4%; Tanaidacea: 58.2 and 60.3%; Isopoda 61.7 and 64.0%; Bivalvia 56.2 and 44.0%). Although this comparison indicated a considerable loss of information when the analysis was restricted to the

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'500 lm size fractions, the high number of samples did not allow analyses of all DISCOL 3 samples at the 250-lm or 300-lm levels. Since DISCOL 1 and DISCOL 2 results were available at the '500 lm level, all data we present in this study refer to this size fraction. In general the 0—5 cm layer is considered for all expeditions; for the DISCOL 3 cruise, data from the 0—10 cm depth range are also presented. Sieve residues were preserved and stored in 4%-formalin solution. In the laboratory, the samples were stained with Rose Bengal, and macrofauna was sorted and identified to high taxa. Groups commonly considered to be meiofaunal taxa were not considered here (e.g. Foraminifera, Nematoda, Harpacticoidea). All Polychaeta were identified to the family level, and, if possible, to the species level. The families Terebellidae, Trichobranchidae and Ampharetidae were difficult to distinguish due to damages during sample processing, and were therefore lumped in the order Terebellida. Abundance counts were generally based on the number of heads, or unequivocally identifiable single animal fragments (provided that double counts of individuals did not occur). The taxonomic analysis revealed 37 polychaete families, with a minimum of 123 sediment-dwelling species living in the DISCOL area (Borowski, 1996). Thirty-nine polychaete species, which allowed facile and unequivocal quantitative species discrimination, were selected for abundance analyses. Initially, we included disturbed, undisturbed, and reference samples as three treatments in the ANOVA, but later realized that we were unable to recognize patterns in the results. For many comparisons, the data required nonparametric methods (i.e. Kruskal—Wallis H-test), and although the ANOVA yielded some significant results, it was often impossible to locate the differences between groups in subsequent multiple comparisons (due to low statistical power). This was especially the case when low abundances resulted in many tied ranks, which reduced the power of nonparametric comparisons. We therefore decided to exclude the reference samples and performed two-tailed comparisons of means between disturbed and undisturbed samples from the DEA. In all comparisons, the tested null hypothesis was: “The abundances in disturbed samples at a given post-impact time do not differ from those in undisturbed ones”. Comparisons were made at higher macrofaunal taxa levels and, for samples that allowed quantitative species discrimination (i.e. DISCOL 2 and DISCOL 3 samples), at polychaete species levels. We only tested within expeditions, because the different methods did not allow comparisons across cruises. We used the t-test in case of homogeneity of variances and normal distribution; otherwise we used the nonparametric Whitney—Mann U-test. Unless stated otherwise, an alpha level of 0.05 was used. Hurlbert’s (1971) rarefaction diversity index was used to measure long term effects on the community structure of polychaetes. In contrast to other studies, we did not strictly use species categories, and not all families were considered. Therefore, our “diversity” results are not comparable to polychaete species diversity in other studies, but they are sufficient to trace long-term effects of disturbance. We calculated E(S ) for n polychaetes from a subset of 14 DISCOL 3 samples (random selection of six disturbed, two undisturbed, and six reference samples; the sediment depth range was 10 cm). We considered families which, to a certain degree, allowed good separation of species. Families, such as Acrocirridae and Spionidae, with high proportions of inseparable

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species and juveniles without sufficient specific characters were omitted. Juveniles were identified to whatever taxonomic level was possible, and remaining specimens were lumped together at the lowest possible taxonomic level (e.g. genus or subfamily). This procedure resulted in a list of 77 “species” (from 23 families) present in the 14 samples. Rarefaction curves of undisturbed and reference samples were compared with those of the disturbed samples. We calculated 95% confidence limits for a mean E(S ) curve from the undisturbed/reference group using the t-distribution and comn pared them to the “disturbed curves”, which were treated as individual observations because of the heterogeneity of their sediments. If a “disturbed curve” fell on or beyond the undisturbed/reference confidence margins, its “diversity” was considered to be significantly different (Smith, 1986; Kukert and Smith, 1992).

3. Results 3.1. Macrofaunal abundances The Polychaeta were the most abundant taxon, constituting 47.0, 53.5, and 52.7%, respectively, of the macrofauna in all samples of the three expeditions, DISCOL 1 (post-impact), 2, and 3. Tanaidacea were the second most dominant group (17.8 17.9, and 20.0%), followed by Isopoda (18.1, 13.4, and 14.2%) and Bivalvia (8.8, 7.5, and 6.5%). Together, these four taxa constituted more than 90% of all macrofauna, while all other groups were of minor importance. In the comparisons of mean abundances in post-impact samples from central and peripheral areas of the DEA, we did not find significant differences (p(0.05) between different areas at any observation time (DISCOL 1—DISCOL 3). We concluded that the plume had not caused significantly different effects on the macrofaunal community within the DEA, and thereafter did not distinguish between different between-track samples. In both disturbed and undisturbed samples, animal densities were highly variable (Fig. 4). The mean macrofaunal densities in undisturbed samples within the DEA (0—5 cm) ranged from 77 (DISCOL 2) to 123 inds./0.25 m2 (DISCOL 3). For all major taxa, the experimental impact resulted in highly significantly reduced abundances in the track areas (Fig. 4, Table 1): Immediately after plowing, the animal densities in disturbed samples were reduced to 38.6% of the undisturbed values. The initial impact intensity was less for the Polychaeta than for the other three groups: After plowing, the polychaete abundances in disturbed samples were reduced to 48.6% of the abundances in undisturbed samples, whereas the Tanaidacea densities were reduced to 28.0% and those of the Isopoda to 18.5%. The Bivalvia, with 9.3%, were nearly eliminated. Half a year after the impact (DISCOL 2), the animal numbers within the disturbed samples were still highly variable (Fig. 4), and the highest disturbed value exceeded even the highest undisturbed one (Table 1). The minimum macrofaunal abundance of 30 inds./0.25 m2 was found in one of two track samples in which semi-liquid material was almost absent. The “disturbed densities” of the Bivalvia were no longer different

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Fig. 4. Mean densities ($S.D.) of the total macrofauna and four dominant taxonomic groups ('500 lm, sediment depth 0—5 cm) in disturbed, undisturbed and reference samples of the three expeditions: DISCOL 1 (post-impact), DISCOL 2, and DISCOL 3. The track samples of DISCOL 2 represent a special case of the disturbed samples, in which semi-liquid surface material was completely absent. Their animal numbers are also included in the bar of the disturbed group. Sample numbers: DISCOL 1 undisturbed: 21, disturbed: 7; DISCOL 2 undisturbed: 22, disturbed: 8, track: 2, reference: 9; DISCOL 3 undisturbed: 20, disturbed: 9, reference: 8.

from undisturbed ones, and those of the Isopoda nearly equaled the undisturbed values. However, the total macrofauna, Polychaeta, and Tanaidacea still displayed lower abundances in the disturbed samples (Table 1). At the reference sites, the animal densities resembled those of the undisturbed sediments in the DEA (Fig. 4). Three years after the impact (DISCOL 3), the animal densities in all sample types exceeded the values of the previous expedition: A maximum of 161 inds./0.25 m2 was

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Table 1 Comparison of means between undisturbed and disturbed samples for the total macrofauna and the major taxonomic groups ('500 lm, as inds./0.25 m2), depth range 0—5 cm after disturbance in March 1989 (DISCOL 1) and September 1989 (DISCOL 2). DISCOL 1 data have been multiplied by four to estimate abundances at 0.25 m2. The statistics are: t"t-test, U"Mann—Whitney U-test. Levels of significance: *"p(0.05, **"p(0.01, ***"p(0.001

DISCOL 1 Total Macrofauna Polychaeta Tanaidacea Isopoda Bivalvia DISCOL 2 Total Macrofauna Polychaeta Tanaidacea Isopoda Bivalvia

n

Mean

S.D.

Median

Min/max

Test

p

Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed

21 7 21 7 21 7 21 7 21 7

85.2 24.5 39.2 14.0 15.6 3.1 16.1 2.3 8.0 0.6

$36.7 $16.9 $19.4 $12.0 $9.5 $3.9 $14.0 $2.4 $4.9 $1.5

76 31 34 12 14 1 13 2 8 0

27/172 1/50 9/84 1/34 0/33 0/9 0/58 0/6 0/16 0/4

t

0.0003***

t

0.003**

U

0.002**

U

0.0006***

U

0.008*

Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed

22 8 22 8 22 8 22 8 22 8

77.0 55.9 40.0 28.0 14.6 8.6 10.0 8.4 6.1 3.4

$16.8 $30.3 $9.3 $14.8 $5.8 $6.0 $5.1 $6.1 $3.4 $0.9

75.5 48.5 38.5 24 15 6 9.5 5.5 6 3

50/108 30/124 29/58 12/55 2/24 4/19 3/20 3/20 1/12 2/5

U

0.011*

t

0.013*

t

0.018*

t

0.75

U

0.065

observed in an undisturbed sample (Table 2). Again, the reference sites had macrofaunal abundances similar to the undisturbed DEA samples (Fig. 4). Temporal variation of macrofaunae abundances at the unaffected reference sites suggests the presence of experiment-independent influences on the population densities. These possibly could result from a change in sample processing methods between expeditions. Increased abundances at DISCOL 3 also could reflect a benthic response to increased organic flux. We observed patches of degraded pelagic diatoms in some of our DISCOL 3 samples, suggesting an earlier pulse of phytodetritus. Differences between “disturbed” and “undisturbed abundances” (p(0.05) were found for total macrofauna, Polychaeta, and two minor groups: Cumacea and Asteroidea (Table 2). However, when we analyzed the 0—10-cm depth range, we did not observe significant differences for total macrofauna and Polychaeta. This indicated higher polychaete densities in the deeper layers of the disturbed sediments, which balanced the observed differences in the top layers. Cumacea and Asteroidea in all samples dwelled closer to the surface, and results were comparable regardless of the depth range of analysis.

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Table 2 Comparison of means between undisturbed and disturbed samples for different macrofauna groups 3 yr after the impact (DISCOL 3, '500 lm, as inds./0.25 m2). Results for the depth ranges 0—5 cm and 0—10 cm are presented separately. Only taxa with significant differences (p(0.05) in at least one of the depth ranges are included. n"Samples. The statistics are: t"t-test, U"Mann—Whitney U-test. Level of significance: *"p(0.05 n

Mean

S.D.

Median

1. Sediment depth 0—5 cm Total Macrofauna Undisturbed Disturbed Polychaeta Undisturbed Disturbed Cumacea Undisturbed Disturbed Asteroidea Undisturbed Disturbed

20 9 20 9 20 9 20 9

122.8 105.1 65.1 52.8 1.6 0.2 0.9 0.1

$17.5 $23.8 $12.6 $12.1 $1.8 $0.7 $1.9 $0.3

121 102 65 56 1 0 1 0

2. Sediment depth 0—10 cm Total Macrofauna Undisturbed Disturbed Polychaeta Undisturbed Disturbed Cumacea Undisturbed Disturbed Asteroidea Undisturbed Disturbed

20 9 20 9 20 9 20 9

144.3 130.9 74.2 66.0 1.8 0.3 0.9 0.1

$22.6 $24.0 $13.4 $12.3 $1.9 $0.7 $1.9 $0.3

139 132 75 69 1 0 0.5 0

Test

p

91/161 69/146 50/96 28/66 0/6 0/2 0/3 0/1

t

0.033*

t

0.02*

U

0.03*

U

0.046*

107/182 93/177 54/109 38/82 0/6 0/2 0/4 0/1

t

0.16

t

0.13

U

0.027*

U

0.046*

Min/max

3.2. Depth distribution in the sediment Three years after the disturbance, the four dominant macrofauna taxa displayed significant differences in their depth distributions (Fig. 5). In undisturbed sediments, most animal groups were concentrated in the upper two centimeters of the sediment, and values around 25% predominated in the 2—5 cm layer. Two-tailed comparison of means between reference and undisturbed DEA samples revealed no significant differences between the sites, except for the Bivalvia in the 2—5 cm layer (Fig. 5). In disturbed samples, depth distributions of all dominant macrofauna taxa were significantly shifted to deeper layers (Fig. 5). Fig. 6 illustrates the small-scale alteration in the colonization structure within a single DISCOL 3 sample, in which we separately subsampled a refilled track and its margin (“Edge”). It shows that the animal densities within the refilled track exceeded those of the undisturbed sediments by about 20—30%. 3.3. Polychaete families Table 3 shows the most important polychaete families ordered by dominance rank for the different sample types at the post impact phases of DISCOL 1, DISCOL 2, and DISCOL 3: Shortly after the impact (DISCOL 1), the Paraonidae were dominant in

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Fig. 5. Depth distribution of the total macrofauna and the dominant taxa ('500 lm) during DISCOL 3 in undisturbed and disturbed DEA-samples and at the southern reference site. Means (bar lengths) and S.D. for relative animal densities in the sediment layers 0—2 , 2—5 , and 5—10 cm; the bar widths represent the vertical ranges of the respective layers. Significant differences between similar depth layers of disturbed and undisturbed samples, or undisturbed and reference samples are represented with asterisks (two-tailed t-test or Mann—Whitney U-test). Levels of significance: *"p(0.05, **"p(0.01, ***"p(0.001.

both sample types, but the subsequent dominance ranks displayed differences between the two types. In disturbed samples, the proportion of the Spionidae was much lower, and a number of families were lacking (e.g. Opheliidae, Syllidae, Goniadidae, Sigalionidae, Lumbrineridae, and Amphinomidae), even though some of them were ranked highly in undisturbed sediments. On the other hand, the dominance of the Cirratulidae and some rare families had dramatically increased (e.g. Capitellidae, Sphaerodoridae, Trochochaetidae, Phyllodocidae (Table 3), and Flabelligeridae). For example, Longosomatidae was absent from undisturbed samples, but reached 5% abundance in the disturbed cores. During subsequent sampling times, the Spionidae were most abundant in all sample types (Table 3). This difference probably was due to the method of subsampling for

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Fig. 6. Depth distribution of the dominant macrofaunal groups three years after the impact in undisturbed sediments and in a track refilled with semi-liquid material. The values for “Edge” and “Track” are derived from subsamples of one box core. Undisturbed values are means of 13 undisturbed and reference samples. The lengths of the bars represent animal numbers for the 500 lm mesh size, transformed from the analyzed depth layers to intervals of 1 cm.

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Table 3 Rank order of the dominant polychaete families ('500 lm) in the different sample types at the expeditions DISCOL 1 (after disturbance), DISCOL 2, and DISCOL 3. Only dominance ranks 1—8 are presented Dominance rank

Reference samples

DISCOL 1 1. 2. 3. 4. 5. 6. 7. 8. ... DISCOL 2 1. 2. 3. 4. 5. 6. 7.

Spionidae Paraonidae Cirratulidae Opheliidae Syllidae Lumbrineridae Acrocirridae

8. ...

Pilargiidae ...

4.1%

DISCOL 3 1. 2. 3. 4.

Spionidae Paraonidae Cirratulidae Opheliidae

26.7% 12.0% 10.6% 6.1%

5. 6.

Syllidae Pilargiidae

5.3% 4.5%

7. 8. ...

Terebellida Acrocirridae ...

3.8% 3.7%

24.9% 13.0% 7.7% 7.1% 5.7% 5.5% 5.2%

Undisturbed samples

Disturbed samples

Paraonidae Opheliidae Spionidae Syllidae Cirratulidae Pilargiidae Goniadidae Nereididae ...

20.0% 12.6% 12.5% 7.9% 6.5% 4.5% 4.0% 3.8%

Paraonidae Capitellidae Cirratulidae Pilargiidae Spionidae Sphaerodoridae Trochochaetidae Phyllodocidae ...

17.9% 14.3% 12.8% 8.6% 8.6% 7.1% 5.7% 5.3%

Spionidae Paraonidae Cirratulidae Opheliidae Lumbrineridae Pilargiidae Acrocirridae Terebellida Syllidae ...

22.5% 15.9% 10.1% 7.6% 4.1% 3.8% 3.5% 3.5% 3.3%

Spionidae Cirratulidae Paraonidae Terebellida Lumbrineridae Syllidae Opheliidae Pilargiidae Acrocirridae ...

23.1% 12.9% 12.0% 6.9% 5.2% 3.8% 3.7% 3.7% 3.5%

Spionidae Paraonidae Cirratulidae Opheliidae Syllidae Acrocirridae Sigalionidae

28.5% 10.7% 7.5% 6.2% 6.2% 4.5% 6.2%

Spionidae Paraonidae Cirratulidae Opheliidae

26.8% 16.5% 9.6% 4.9%

Lumbrineridae Terebellida ...

3.6% 3.2%

Lumbrineridae Capitellidae Syllidae Pilargiidae Maldanidae ...

4.8% 3.0% 2.9% 2.9% 2.8%

the smaller macrofauna during DISCOL 1, which may have damaged the usually small and fragile Spionidae. Half a year after the impact, the dominance order in the disturbed samples was still affected: The importance of the Cirratulidae and the Terebellida was still elevated, whereas the Paraonidae ranked third. Three years after the impact, these differences had more or less disappeared, and the arrangement of the higher ranks in the disturbed samples resembled the undisturbed and the reference sites.

C. Borowski, H. Thiel / Deep-Sea Research II 45 (1998) 55—81

71

3.4. Comparison of means for selected polychaete species The detection of single species reactions to the disturbance was hampered by low densities. In the later post-impact phases (DISCOL 2 and DISCOL 3), only 10 of 39 selected species showed differences in abundance between undisturbed and disturbed samples (Table 4). During DISCOL 2, significant effects were only detected for two species. The abundances of both the goniadid Progoniada sp. A and the paraonid Paraonella abranchiata were significantly reduced in the disturbed samples. Paraonella abranchiata also displayed a week signal at DISCOL 3. However, in contrast to DISCOL 2, this species was slightly more abundant in disturbed samples rather than reduced. This pattern also was observed at even higher significances for the amphinomid Paramphinome sp. A. Seven other species apparently were affected in the disturbed DISCOL 3 samples. The opheliid Ophelina abranchiata, the sigalionid ¸eanira sp. A, and the syllids Braniella cf. palpata and Exogone sp. B displayed lower abundances in the top 5 cm. For all these species, disturbance effects were not significant over a depth range of 0—10 cm. This suggested higher colonization rates of these species in deeper layers of the disturbed sediments. The significant result for the nephtyid Micronephtys sp. A was not influenced by the sediment depth (Table 4). The sigalionid ?Psammolyce sp. A and the syllid ?Brania sp. A were absent from disturbed samples (Table 4). However, these species also were extremely rare in undisturbed sediments, and the significance of the results very likely was biased by the low densities. 3.5. “Diversity” patterns The Hurlbert-rarefaction results demonstrate sustained effects of the disturbance on the polychaete fauna during DISCOL 3 (Fig. 7). The reference and undisturbed curves lie close together and their steep slopes indicate similar high “diversity”. The curves of the disturbed samples are more widely dispersed, with curves falling within and below the 95% confidence limits. Two curves display significantly reduced “diversity”.

4. Discussion The aim of the DISCOL program was to investigate the recolonization of the deep-sea bottom after physical disturbance, as would be expected from anthropogenic impacts, such as nodule mining or the disposal of waste. Since it is not likely that these impacts will eliminate all deep-sea fauna, the DISCOL experiment did not intend to defaunate the sediments, but aimed at disturbing the benthic community on a large scale. Previous colonization experiments in the deep sea were designed for small-scale experimental fields of a few square decimeters. These experiments deposited artificial sediment mounds or exposed colonization trays with azoic sediments or artificial

Paramphinome sp. A

Micronephtys sp. A

Exogone sp. B

Braniella cf. palpata

?Brania sp. A

?Psammolyce sp. A

¸eanira sp. A

Ophelina abranchiata

DISCOL 3 Paraonella abranchiata

Progoniada sp. A

DISCOL 2 Paraonella abranchia

Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed Undisturbed Disturbed

20 9 20 9 20 9 20 9 20 9 20 9 20 9 20 9 20 9

Undisturbed 22 Disturbed 8 Undisturbed 22 Disturbed 8

n

3.2 5.1 1.3 0.1 1.8 0.6 0.5 0 0.3 0 1.6 0.3 1.2 0.6 1.1 0.4 1.3 2.3

2.8 0.6 0.5 0.0

Mean

$2.3 $2.8 $1.1 $0.3 $1.6 $0.9 $0.7 $0 $0.6 $0 $1.4 $0.7 $0.8 $0.5 $0.9 $1.0 $1.2 $1.3

$1.5 $0.7 $0.7 $0

S.D.

3 5 1 0 1 0 0 0 0 0 1.5 0 1 1 1 0 1 2

3 0.5 0 0

Median

Sediment depth 0—5 cm

0/10 1/9 0/3 0/1 0/5 0/2 0/2 0/0 0/2 0/0 0/4 0/2 0/2 0/1 0/3 0/3 0/4 0/5

1/6 0/2 0/2 0/0

U

U

U

U

U

U

U

U

t

U

U

Min/max Test

0.04*

0.029*

0.059°

0.016*

0.11

0.047*

0.035*

0.004**

0.062°

0.035*

0.0006***

p

3.4 5.6 1.3 0.4 1.8 0.8 0.5 0 0.4 0 1.6 0.4 1.4 0.9 1.1 0.4 1.7 3.1

Mean

$2.5 $3.1 $1.1 $0.7 $1.6 $0.8 $0.7 $0 $0.6 $0 $1.4 $1.0 $0.9 $1.1 $0.9 $1.0 $1.8 $1.5

S.D.

3 5 1 0 1 1 0 0 0 0 1.5 0 2 1 1 0 1 3

Median

Sediment depth 0—10 cm

0/11 2/11 0/3 0/2 0/5 0/2 0/2 0/0 0/2 0/0 0/4 0/3 0/3 0/3 0/3 0/3 0/7 1/6

U

U

U

U

U

U

U

U

t

Min/max Test

0.027*

0.029*

0.21

0.21

0.071°

0.047*

0.1

0.047*

0.061°

p

Table 4 Polychaete species from DISCOL 2 and DISCOL 3 ('500 lm, as inds./0.25 m2): Comparison of mean abundances in undisturbed and disturbed samples. Only species with at least low level significant results (p(0.1) are presented. n"Samples. The statistics are: t"t-test, U"Mann—Whitney U-test. Levels of significance: °"p(0.1, *"p(0.05, **"p(0.01, ***"p(0.001

72 C. Borowski, H. Thiel / Deep-Sea Research II 45 (1998) 55—81

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Fig. 7. Hurlbert rarefaction curves for polychaete “diversity” of single box-core samples during DISCOL 3, on the basis of 77 “species” ('500 lm, 0—10 cm sediment depth). (A) undisturbed and reference samples; (B) solid curves represent disturbed samples, the dotted curve is the calculated mean for the undisturbed/reference group with 95% confidence limits. The hatched lines represent theoretical maximum diversity.

substrates on the deep-sea bottom (Grassle, 1977; Desbruye`res et al., 1980, 1985; Grassle and Morse-Porteous, 1987; Levin and Smith, 1984; Smith et al., 1986; Kukert, 1991; Kukert and Smith, 1992; Snelgrove et al., 1992, 1994). The exposed sediments usually originated from the experimental sites and were defaunated by freezing and homogenizing in the laboratory before their deployment with the trays (Grassle, 1977; Grassle and Morse-Porteous, 1987). In some cases, the substrates were additionally organically enriched (Desbruye`res et al., 1980, 1985; Levin and Smith, 1984; Snelgrove et al., 1992, 1994). The comparison of such tray experiments with DISCOL is limited, as their designs, which frequently isolated the sediments from the surrounding sea floor in elevated trays, biased the mode of the colonization in various ways (Smith, 1985; Snelgrove et al., 1992, 1994). In contrast to these experimental approaches, DISCOL did not install well-defined artificial environments with defaunated and homogenized sediments. The in situ operated plow-harrow created physical disturbance of varying intensity in different areas, as is expected to result from an industrial operation. High mortality was expected within the disturber tracks where the fauna was impacted by direct contact with the plow-harrow or by shearing of sediments, and where the near-surface fauna was resuspended within the sediment plume. In addition, overturning of sediments partially buried fauna within the tracks and at track margins, no doubt contributing further to mortality. In areas between tracks, plume redepostion must have caused much less mortality (Fig. 4). 4.1. Early effects in the tracks: DISCO¸ 1 Jumars (1981) hypothesized that manganese nodule mining could cause as much as 95% mortality of benthic fauna in the collector tracks. However, deep-sea data were

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not available at that time. The faunal densities in the disturbed DISCOL 1 samples were reduced to 9.3% for the Bivalvia, 28.0% for the Tanaidacea, 18.5% for the Isopoda, and 48.6% for the Polychaeta. These values are not quite as high as Jumars predicted, perhaps because most disturbed DISCOL samples were not collected in the middle of a track. Many samples also contained undisturbed sediment areas, which may have inflated the overall “disturbed abundances”. The DISCOL treatment effects for the Bivalvia and the Crustacea are comparable to effects from shallow-water investigations of the impacts of fishery activities on the benthos. Heavy impacts on endo- and epibenthic fauna, i.e. on Mollusca, Decapoda, Echinodermata, and Polychaeta, which are not adapted to high-energy environments, have been demonstrated in mussel-dredging investigations (Eleftheriou and Robertson, 1992). Numerous studies have confirmed the negative impacts of trawl and beamtrawl fisheries on Echinodermata, Polychaeta, Crustacea, and especially on Bivalvia (Arntz and Weber, 1970; Medcof and Caddy, 1971; Caddy, 1973; Bergman et al., 1990; Bergman and Hup, 1992). The mortality of the bivalve Arctica islandica in the tracks of an experimental beamtrawl investigation in the North Sea was 90% (BEON, 1990, 1992, cit. after Hall, 1994). These shallow water data are strikingly similar to the DISCOL results. The relatively moderate impact on the Polychaeta of the DISCOL treatments may be due to a high survival rate for particular species. Especially large individuals of deep-burrowing species may have escaped, as the high dominance of Paraonidae, Cirratulidae, Capitellidae, Pilargiidae, and Longosomatidae would suggest. These families include relatively large burrowing species of the genera Aricidea, ¹haryx, Chaetozone, Heterospio, Notomastus, and Sigambra, which in selected undisturbed DISCOL samples occasionally were found in sediment layers below ten cm. (Borowski, 1995, 1996). Families with smaller body sizes and shallower dwelling habits were less dominant in the disturbed samples (e.g. Spionidae and Opheliidae). The motility of the Polychaeta probably allowed rapid recolonization from outside of the tracks. Smith et al. (1986) reported rapid macrofaunal recolonization of artificial sediment mounds in the bathyal Santa Catalina Basin (SCB), where after 50 days the macrofaunal abundances had already reached 52—85% of the background community. They concluded that recolonization in artificial mounds, which allows horizontal immigration from surrounding sediment, leads to 10-fold faster recolonization rates than earlier tray experiments in the same region had demonstrated. Kukert (1991) and Kukert and Smith (1992) in similar mound experiments found high resistance of the SCB macrofauna towards sudden burial under sediment layers of 5—6 cm and recognized vertical migration as the predominant colonization mode in the deposited mounds. Smith (1986) assumed high dispersal rates over meter scales compared to general population growth rates in deep-sea areas. The disturbed DISCOL 1 samples were obtained within 28—40 days after the beginning of the plowing, i.e. after a period of time that was long enough to allow initial recolonization in the earliest created tracks. Although the DISCOL tracks were 8 m wide in total, most samples were obtained from areas where disturbed sediments bordered undisturbed ones. Thus, rapid recolonization by lateral migration of motile macrofauna (e.g. Capitellidae, Cirratulidae, and Pilargiidae) was very likely.

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It should be stressed again that the above mentioned artificial-mound experiments were performed in the bathyal SCB ((1300 m) where natural disturbances likely happen more frequently than in abyssal oceanic basins. Biogenic burial of the macrofauna under sediment mounds produced by abundant echiurids are a common phenomenon in the SCB (Smith, 1986; Smith et al., 1986; Kukert and Smith, 1992), but not in the DISCOL area. It is unclear to what extent SCB results are applicable to the DISCOL area, and therefore it is not clear whether the macrofauna in the disturbed samples of the initial post-impact sampling phase were survivors or colonists. 4.2. The macrofauna between the tracks Redeposited material from the sediment plume was recognized in video observations over large areas of the DEA (Bluhm et al., 1995), but we were not able to detect negative effects on the macrofaunal abundance because we could not compare pre-impact and post-impact data. However, we did not find differences between the putative more heavily impacted central area and the periphery of the DEA, and animal abundances in unplowed sediments inside and outside the DEA did not indicate sustained effects (Fig. 4). The majority of the sediment-dwelling Polychaeta in the DISCOL material were burrowing or tube-dwelling deposit feeders (Borowski, 1996), and many deep-sea Tanaidacea and Isopoda also are deposit-feeding infauna (Reidenauer and Thistle, 1985; Thistle et al., 1985; Thistle and Wilson, 1987). Filter feeders are considered to be most sensitive towards heavy sedimentation (Rhoads and Young, 1970; Jumars, 1981), and among the DISCOL Polychaeta suspension feeders appear to be rare (Borowski, 1996). We assume that the large-scale impact of the plume was too low to detectably affect the macrofauna, and that the majority of the DISCOL macrofauna was sheltered under the sediment surface when the plume resettled, and therefore protected from ill effects. 4.3. Later observations on recolonization of the tracks Thiel (1992a) and Bluhm et al. (1995) predicted time scales of years to several decades for the faunal recovery of large-scale, physically disturbed, manganese-nodule areas. Fast recolonization of the disturbed DISCOL sediments in the early postimpact phase seems to contradict these predictions. However, macrofaunal depth distributions in disturbed samples indicated continued disturbance during DISCOL 3. The Hurlbert rarefaction patterns at the polychaete “species” level suggest that species associations in disturbed samples 3 yr after the impact still differed from unimpacted sediment. A high degree of heterogeneity within the disturbed samples and significant low “diversities” of single samples indicated persisting long-term effects of the disturbance. The increased dominance rank of cirratulid Polychaeta in the tracks half a year after the disturbance suggests opportunistic abundance increase by r-selected reproduction of certain species. Unusually high abundances of certain cirratulid species is well documented from organic polluted shallow waters (Pearson and Rosenberg,

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C. Borowski, H. Thiel / Deep-Sea Research II 45 (1998) 55—81

1978) and was also demonstrated for physically disturbed deep-sea sediment (Smith et al., 1986). However, such an opportunistic response was not observed for any examined species in the DISCOL material. Moreover, the majority of all tested species was equally distributed in disturbed and undisturbed sediments only half a year after the disturbance. The unusual reaction of the paraonid species Paraonella abranchiata does not allow unequivocal interpretation: P. abranchiata was previously only reported in a single nonquantitative deep-water study from the North Pacific (Fauchald and Hancock, 1981), and the ecological demands of this species are unknown. High recolonization rates that do not result from opportunistic reactions of a few r-selected species contradict the results of small-scale tray experiments. (1) When the trays were deployed without artificial organic enrichment, low colonization rates occurred. For example, Grassle and Morse-Porteous (1987) recovered their trays after seven months at 3600 m in the western North Atlantic and obtained only 10—15% of the species densities and the animal abundances observed in the background community. Treatments with the longest exposure time of 59 months increased to 60—70% of both parameters. Other tray experiments, in which lateral migration was excluded, also showed far lower colonization rates than the DISCOL results (Grassle, 1977; Levin and Smith, 1984; Desbruye`res et al., 1985). (2) When trays where organically enriched, high colonization rates of a few species were observed (Desbruye`res et al., 1985; Snelgrove et al., 1994). These examples suggest different processes in the colonization of small-scale, isolated tray treatments versus the recolonization of sea-floor sediments disturbed over large scales. Higher colonization rates in the DISCOL sediments than in the unenriched tray treatments in part may be explained by different levels of defaunation (partial in DISCOL versus total in trays). In addition, the high recolonization rates of the DISCOL tracks point to the importance of lateral migration from surrounding sediments, rather than the settlement of larvae. Experiments with artificial sediment depressions and artificial sediment mounds support the importance of migration: Snelgrove et al. (1994) tested the colonization of artificial sediment depressions and found significantly higher abundances of burrowing organisms than in nearby control trays. At least for burrowers, this indicated faster colonization rates by lateral migration in the sediment than by invasion through the water column. Some of Kubert and Smith’s (1992) mounds were deposited on plates to inhibit immigration from the underlying sediment. These “floored mounds” had significantly lower colonization rates, in terms of animal abundances and species densities, than “unfloored mounds”. The colonization rates of the “unfloored mounds” were comparable to the DISCOL data, whereas the “floored mounds” yielded results similar to the tray experiments. 4.4. The semi-liquid layer The possible importance of the semi-liquid surface sediments for rapid recolonization was implicated in the results from the disturbed DISCOL 2 samples. High colonization densities were observed where furrows and crevices between the

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sediment blocks had already filled up with soft material, while very low macrofauna abundances were obtained from two track samples in which semi-liquid material was absent. The regeneration of the semi-liquid surface layer apparently is mainly caused by horizontal transport of plowed up and destabilized sediments with near-bed currents. No erosion measurement data are available from the deep sea, and almost all near bottom current measurments have been conducted several decimeters or meters above the seafloor. Some rather general statements suggest that near-bed currents with velocities '10 cm/s may mobilize fine pelagic sediments (Heezen and Hollister, 1971; McCave, 1984, cit. after Paterson and Lambshead, 1995), but these assumptions would not apply to a disturbed area, where the sediment-surface stabilizing bacterial film is interrupted. The tracks and fissures between the broken up sediments affect near-bed hydrodynamics and may cause increased sedimentation of transported fine grained particulate material. Altered hydrodynamics in natural depressions of the deep-sea bed (Nowell and Jumars, 1984; Snelgrove et al., 1993, 1994) can cause accumulations of organic material that ranges from phytodetritus to macroalgae (Sokolova, 1972; Thiel et al., 1988/89; Grassle and Morse-Porteous, 1987). An additional factor may be the horizontal transport of surface sediment caused by bioturbation (in contrast to vertical mixing bioturbation, which is mostly considered under this term). Photographic results from deep-tow systems and long-term camera observations (Bluhm and Thiel, unpubl. observ.) demonstrate suspension of surface sediment by only slowly swimming fish. Demersal fish shift sediment by their fin movements or body wriggling. Holothurians introduce deep tracks into newly redeposited plume sediments. The abundant decapod Probecbei mirabilis is a good runner, and thus should shift sediment to the side. Other decapod species, asteroids and ophiurids burrow in the sediment surface. These actions shift sediment sidewise and thus fill up depressions, holes, and fissures; they may also sediment into shallow mounds or bulges, creating near surface roughness that may be eroded by week currents. This bioturbation should have stronger effects after mechanical disturbance and resedimentation, when the sediment surface consists of a very loose particle structure. One reason for the attractiveness of accumulated semi-liquid surface sediments for recolonization may be their potentially high content of food particles. Although the amount of organic carbon at undisturbed sites in the DISCOL area increases with sediment depth, the chemical reactivity of this organic carbon is highest near the sediment surface and decreases with depth (I. Ko¨nig, unpubl. data). Chemical reactivity of organic matter generally decreases with time (Middleburg, 1989) and the relatively freshly deposited labile organic matter near the sediment surface should provide the major food source for deposit feeders. It is this plowed up surface material that is expected to accumulate in the plow-harrow tracks. A possible explanation for high animal abundances of some disturbed samples lies in the vertical extent of the semi-liquid layer. The DISCOL 3 data suggest that the macrofauna in refilled tracks could exploit deeper sediment layers than in undisturbed sediments. Burrowers like Paraonella abranchiata, Ophelina abranchiata, and Paramphinome sp. A are examples for species which may have profited from the changed sediment conditions in deeper layers.

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5. Conclusions and speculations The recolonization by macrofauna of the DISCOL tracks took less time than we originally predicted based on the concept of slow biological processes in the deep sea. Previous tray experiments using isolated azoic sediments are thought to simulate disturbance patch sizes too large to be recolonized by lateral migration, so that recolonization occurs exclusively by larval settlement (Grassle, 1994). As the main mode of macrofaunal recolonization in the DISCOL tracks apparently was lateral migration, we conclude that our disturbance experiment, although designed on a large scale, for the macrofauna only created small-scale disturbed patches, leaving enough nearby undisturbed areas to facilitate recolonization from lateral migration. Future industrial activities are likely to yield more harmful impacts to the benthic community than we created with our experiment: e.g. commercial manganese nodule mining tracks, for economical reasons, will likely meander in narrow and overlapping loops, and they will be closer together than those of the plow-harrow in the DEA. Unmined strips should be narrow. These would receive most probably thick cover of redeposited sediment. The mined areas are assumed to be 20—100 km2, and disturbance will reach deeper into the sediment column. Although a certain lateral recolonization potential may exist from the smaller “undisturbed” areas between industrial collector tracks, this certainly will be lower than in the DISCOL experiment. The recovery potential of an industrially disturbed community will probably depend on the reestablishment of the semi-liquid surface sediments. This process, however, appears to be influenced by the local hydrodynamic regime and may take longer in other abyssal regions. In addition, industrial track densities will result in much more resuspended material which may also affect burrowing infauna via burial disturbance. In such regions, we expect disturbance to persist for longer times.

Acknowledgements We thank the crew of R.V. Sonne and all colleagues who helped to collect and process the samples (i.e. B. Bloemeoke, C. Bussau, F. Buhs, E.J. Foell, D. Gross, G. Hoffmann, J. Klein, K. Knickmerer, H. Kukert, Lin Lu, U. Luth, C. Moybarg, K. Phillips, C. Peters, L. Schmittmann, A. Sommer, G. Thiel, V. Tilot, R. Velten, K. Vopel, K. Watson and U. Wilhelmsen). Thanks to U. Gerloff, C. Hrack, I. Ihole, A. Nemeyer and G. Schwarz for their help with sample sorting. We are grateful to C.R. Smith for a fruitful discussion and very helpful comments on the manuscript. Two anonymous reviewers contributed considerably to the improvement of this manuscript. Thanks to N. Dubilier and C.R. Smith for streamlining the English. The DISCOL program was funded by the Bundesminister fu¨r Forschung and Technologie of the Federal Republic of Germany through contracts 03-R-389, 03-R-392, 03-R-411, and 03-F-0010. The authors are responsible for the content of this paper. This is contribution no. 1302 from the Alfred Wegener Institute for Polar and Marine Research, Germany, and DISCOL publication no. 49.

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