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The role of Callianassa subterranea (Montagu) (THALASSINIDEA) in sediment resuspension in the North Sea
Continental Shelf Research 18 (1998) 1365 — 1380
The role of Callianassa subterranea (Montagu) (THALASSINIDEA) in sediment resuspension in the North Sea A.A. Rowdena,b,*, M.B. Jonesa, A.W. Morrisb a
Department of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK b Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, UK
Received 8 October 1992; received in revised form 17 November 1994; accepted 13 March 1998
Abstract The mud shrimp Callianassa subterranea (Montagu) is a common member of the macrobenthic community at the site in the North Sea selected to study the dynamics of suspended sediment behaviour. The extensive burrowing habit of this deposit-feeding species makes it an important contributor to the degree of bioturbation experienced at the site. Individuals recovered from the site were returned to the laboratory to investigate the influence of body size and temperature upon the amount of sediment expelled. A clear relationship between these variables and the quantity of expelled sediment was identified, and a well-defined temporal pattern of expulsion activity and inactivity was demonstrated. These experimental data, together with field information on seawater temperatures and aspects of mud shrimp population dynamics, allow the construction of an estimated annual sediment turnover budget of 11 kg (dry weight) m~2 yr~1. Field observations at the North Sea site show that the sediment expelled by the mud shrimp forms unconsolidated volcano-like mounds, which significantly modify seabed surface topography. The dimensions of these surface features were measured from bottom photographs of the site and used to determine values of boundary roughness length (Zo). In January Zo was 0.0007 cm, whilst in September Zo equaled 0.79 cm. Callianassa subterranea’s maximum contribution to resuspension was assessed by calculating a derived lateral sediment transport rate of 7 kg m~1 month~1 (from values of near-bed current velocity, modified boundary roughness length and sediment turnover rate). ( 1998 Elsevier Science Ltd. All rights reserved
* Corresponding author. 0278—4343/98/$ — See front matter ( 1998 Elsevier Science Ltd. All rights reserved PII: S 02 7 8— 4 34 3 ( 98 ) 0 00 4 8— X
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1. Introduction The diverse activities of marine benthic organisms resulting in sediment turnover (or reworking) have been a focus of study since the importance of animal—sediment relationships was reviewed by Rhoads (1974). Such bioturbation may alter the geotechnical properties of sediment (Richards and Parks, 1976; Rhoads and Boyer, 1982), affect physical and chemical processes at the sediment—water interface (Aller, 1978), and influence faunal community structure (Myers, 1977; Brenchley, 1981; Posey, 1986). Most major phyla have representatives capable of processing and transporting large quantities of sediment via activities such as feeding and burrowing in both subtidal and intertidal habitats; however, thalassinid crustaceans appear to be dominant sediment reworkers wherever they exist in moderate abundance (for review see Lee and Swartz, 1980). The thalassinid shrimp Callianassa subterranea (Montagu, 1808) is a burrowing deposit feeder, with a wide distribution around the coastal waters of northern Europe from the Mediterranean Sea to the coast of Norway (de Man, 1928; Christiansen and Greve, 1982). In the North Sea, C. subterranea is restricted to water depths of between 30—50 m, where it occurs in muddy-fine sand in densities ranging between 2 and 60 individuals m~2 with a mean of 22 m~2 (Kunitzer et al., 1992). The aims of the current investigation were to quantify the sediment turnover rates for this important bioturbatory species and to evaluate the significance of such activity for sediment resuspension. The work formed part of an interdisciplinary study within the U.K.’s Natural Environment Research Council’s North Sea Project (1987—1992), and developed from a companion study which aimed to identify the influence of benthic macrofauna on the geotechnical and geophysical properties of surficial sediment (Rowden et al., 1998).
2. Materials and methods 2.1. The study site For location and physical characteristics of study site, see Morris and Howarth (1998). 2.2. Shipboard sampling and laboratory sample treatment Macrofauna and sediment — see Materials and Methods section of Rowden et al. (1998). Population structure of Callianassa subterranea — see Materials and Methods section of Rowden and Jones (1994). Seabed photography — In January, May and September 1989, a seabed photographic survey of the site was completed using a ‘cage-type’ UMEL underwater camera assembly. The instrument was deployed 5 times at each station and ‘fired’ automatically 23 cm above the seabed by a contact weight trigger. The survey was conducted at times of lowest tidal current speed to ensure maximum
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potential imaging. Calibration trials with the camera assembly, arranged as per field deployment, allowed the total area and depth of field of view to be calculated, plus the relationship between an object’s imaged and real height/width. Measurements on the negatives were made with the aid of sliding calipers ($0.1 mm) and a stereoscopic microscope (]20). 2.3. Sediment turnover estimates for callianassa subterranea Collection and maintenance — Experimental animals and sediment were collected in April and July 1990 from the station at the centre of the one square sea mile study site. Ten box cores were taken to ensure sufficient animals and sediment to stock laboratory microcosms. Shrimps were hand sorted, placed individually into 1 l pots containing native sediment and seawater, and housed in a constant temperature room adjusted to ambient seawater temperature for the duration of the cruise (2 weeks). Seawater was replaced at 48 hourly intervals. Sediment was frozen aboard the ship to achieve defaunation. During transport to Plymouth (8 h journey), the animals were packed in an insulated container with quantities of ice, whereas the native sediment was uninsulated and refrozen on arrival for storage. 2.3.1. Laboratory design Callianassa subterranea of known sex and size (6.0—10.5 mm carapace length) were placed individually into microcosms made from grey-plastic tubing with wooden bases. Each microcosm measured 30 cm (diameter) by 40 cm (depth) and approximated the natural space requirements of individual animals at the study site (site mean"19 adult shrimps m~2"0.05 m2 individual~1, microcosm surface area "0.07 m2; for population details see Rowden and Jones, 1994). The microcosms, containing native sediment which had been allowed to ‘settle’ for two weeks prior to the introduction of the animals, were arranged within a large tank (approx. 3 m]1 m) of circulating seawater at the temperature encountered at the collection site. The experiment was conducted on three separate occasions using fresh animals acclimatised to the temperatures experienced at the study site in January (7°C), May (9°C) and September (15°C), 1989. 2.3.2. Sample collection and treatment Almost immediately after introduction to the sediment, each animal began to burrow, and records of the burrowing behaviour and surface features produced by the animals were taken at daily intervals. The day after disappearance beneath the sediment surface (deemed day 1), all pseudofaecal and faecal material expelled to the surface was collected (daily for the first seven days, twice weekly thereafter for the experiments at 9 and 15°C, and monthly for those at 7°C). When the exhalant opening of the burrow became conspicuous, a collector (130 ml dessert pot with a hole in its base) was placed over the exit. Expelled material was easily and accurately removed with the aid of a large syringe (60 ml). The collected material was decanted into
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separate pots (250 ml), vacuum filtered (Whatman GF/C 9 mm), washed to remove salt, dried (100°C overnight) and weighed (Sartorius R200D balance -$0.01 g). Opportunistic observations (n"20) were made of the height to which sediment was ejected by the shrimps. The height of the ejection plume was measured by reference to the wall of the collector.
3. Results 3.1. Site characteristics For details of the site’s faunal and sediment geotechnical/geophysical characteristics see Rowden et al. (1998). 3.2. Callianassa subterranea population structure, distribution and density No Callianassa subterranea were recovered in January 1989. This ‘absence’ may be an artefact, as the relatively shallow sampling carried out at that time would not have reached their burrowing depth in colder months (Witbaard and Duineveld, 1989). A restricted quantitative study was undertaken in May 1989 (only sub-cores were sieved), so no suitable data are available for this month. Analysis of C. subterranea numbers in the five box cores taken at the study site for each of the following five visits, showed that individuals were contagiously (patchily) distributed (i.e. the variance is significantly greater than the mean) amongst the samples for October, April and August. In September and July, the distribution was not significantly different from random. Clearly, more samples are required to establish conclusively the within-site distribution of C. subterranea; however, variation in mean density between months was small (38—59 m~2), implying that the population was relatively stable over time, with a mean site density of 46 m~2 (1SD"$8) (for more detail see Rowden and Jones, 1994) 3.3. Sediment turnover estimates for callianassa subterranea 3.3.1. Pattern of sediment expulsion The expulsion activity experiment was designed to calculate the total amount of material expelled to the sediment surface by the Callianassa subterranea population at the North Sea study site via extrapolation of the measured expulsion rates of individuals of known size and sex. The initial construction of the burrow entailed the highest expulsion rates (omitted from subsequent analysis), after which the animal maintained its burrow structure by the ejection of unwanted material during regular and discrete periods of expulsion activity (Fig. 1). These active periods can be most easily characterised by the nature of the time which separates them — deemed ‘inactive periods’ or ‘periods of inactivity’. The periodicity of these inactive periods was defined by calculating the mean duration and frequency of such events for each test animal [duration was simply identified as the mean number of days of inactivity,
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Fig. 1. Sediment expulsion behaviour of the mud shrimp Callianassa subterranea over time (representative example; male, carapace length of 9.5 mm).
whilst frequency was measured as the average occurrence of inactivity in a calender month]. A significant relationship existed between the size of C. subterranea and both components of the inactive periods for individuals maintained at both 9°C and 15°C (Figs. 2A and B). With increasing body size, the periods of inactivity became longer and less frequent. Very little sediment was ejected by C. subterranea kept at 7°C and the consequent low collection frequency did not allow for any description of expulsion behaviour. 3.3.2. Daily expulsion rates Mean daily expulsion rates were calculated for each individual test animal for the periods when Callianassa subterranea was actively ejecting sediment. The results show that the amount of material expelled to the surface mounds was related significantly to size and temperature (Fig. 3). Smaller animals produced less faeces and pseudofeaces than larger ones, and animals experiencing the summer temperature (15°C) expelled greater quantities than those experiencing both the spring (9°C) and winter temperatures (7°C) (ANCOVA; F-ratio"3.893, df"2, 12, P"(0.05). 3.3.3. Monthly sediment processing calculation The population size structure of Callianassa subterranea at the study site, together with the results of the expulsion activity experiment, allow an estimation of the amount of particulate material expelled to the sediment surface by the burrowing and feeding activities of these animals for each of the three study months (Table 1). Regression-derived values for frequency and duration of inactivity enables calculation of the number of days that a shrimp of a particular size actively expels sediment. For example in September, an individual with a carapace length of 6.5 mm had an inactive
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Fig. 2. The relationships between the size of the mud shrimp Callianassa subterranea and the inactive periods of sediment expulsion behaviour, A. Duration (May, r"0.812 P"0.02; September, r"0.911 P"0.001), B. Frequency (May, r"!0.91 P"0.003; September, r"!0.690 P"0.05).
period of 3.53 days which occurred 2.13 times each month. Hence, the amount of time an animal of this size actively expels sediment in a month may be estimated [e.g. for September, 30—(3.53]2.13)"22.48 days]. The monthly expulsion rate for individuals is calculated by multiplying this value by the daily expulsion rate for an animal of a corresponding size, also regression derived [e.g. for September, 6.5 mm: 22.48]3.01"67.66 g (dry weight) month~1]. This rate, when combined with the measured density of C. subterranea, enables a value for expelled sediment per unit area to be achieved [e.g. for September, 6.5 mm: 67.66]2.4"162.38 g (dry weight) m~2 month~1]. Finally, for the larger shrimps, the results of such calculations are summed to give an estimate of the total amount of material the population was responsible for expelling to the sediment-water interface. This results in values of 2.8 kg
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Fig. 3. The relationships between the size of the mud shrimp Callianassa subterranea and sediment expulsion rate, for three experimental temperatures (January, r"0.976 P"0.008; May, r"0.734 P"0.05; September, r"0.824 P"0.02).
(dry weight) m~2 month~1 for September, 0.4 kg (dry weight) m~2 month~1 for May and 0.06 kg (dry weight) m~2 month~1 for January. [Large C. subterranea (6.0— 11.0 mm carapace length) represent a significant proportion of the population’s weight or biomass (e.g. 94% in September; Rowden, 1993) and are also likely to account for almost all of the sediment expelled to the surface as small animals are not thought to be extensive burrowers (Witbaard and Duineveld, 1989)]. 3.4. Calculation of an estimated annual sediment expulsion budget From a non-linear quadratic regression of the sediment expulsion rates (calculated for each of the three study months) against temperature it is possible to obtain estimates corresponding to temperatures between 6—15°C. Combining these predicted values with the monthly seawater temperatures measured at the site during 1989 (BRITISH OCEANOGRAPHIC DATA CENTRE, 1992) an estimated annual pattern of Callianassa subterranea sediment expulsion is obtained (Fig. 4). The model illustrates that the shrimps expel relatively negligible quantities of sediment during the months of January to April [(0.06 kg (dry weight) m~2 month] before they begin to increase output steadily through the spring and early summer [e.g. July"1.3 kg (dry weight) m~2 month~1]. The maximum expulsion rate is achieved at the end of the summer [September"2.8 (dry weight) m~2 month~1], then activity decreases through the autumn before sediment expulsion returns to more modest rates, corresponding to the lower temperatures experienced at the year’s end [December "0.4 kg (dry weight) m~2 month~1]. The summed monthly estimates predict a total annual sediment expulsion of 11 kg (dry weight) m~2 year~1 for C. subterranea at the study site.
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Table 1 Sediment expulsion determinations for the three study months Shrimp size (carapace length -mm)
Sediment expelled in a day (g day~1)
Duration of inactive periods (days)
Frequency of inactive periods (times)
Duration of active period in a month
Sediment expelled in a month (g month~1)
Site shrimp density (indiv. m~2)
Site sediment turnover rate (g m~2 month~2)
January (7°C) 6.0 0.11 — 6.5 0.12 — 7.0 0.13 — 7.5 0.14 — 8.0 0.15 — 8.5 0.16 — 9.0 0.17 — 9.5 0.18 — 10.0 0.19 — 10.5 0.20 — 11.0 0.21 — Total"61.96 g m~2 month~1
— — — — — — — — — — —
24.94 23.29 21.94 20.84 20.02 19.47 19.17 19.14 19.38 19.93 20.70
2.67 2.75 2.81 2.90 2.98 3.12 3.26 3.46 3.70 4.03 4.39
0.40 0.40 2.40 2.80 1.60 1.60 0.40 3.60 4.40 0.40 0.80
1.07 1.10 6.74 8.11 4.77 4.98 1.30 12.47 16.29 1.61 3.51
May (9°C) 6.0 0.70 1.62 6.5 0.85 2.49 7.0 1.01 3.35 7.5 1.16 4.22 8.0 1.32 5.09 8.5 1.47 5.95 9.0 1.63 6.82 9.5 1.78 7.69 10.0 1.94 8.55 10.5 2.09 9.42 11.0 2.25 10.29 Total "378.95 g m~2 month~1
2.94 2.78 2.61 2.45 2.29 2.13 1.97 1.81 1.64 1.48 1.32
26.24 24.09 22.24 20.65 19.35 18.33 17.59 17.12 16.94 17.03 17.41
18.29 20.52 22.40 24.00 25.48 26.98 28.62 30.51 32.81 35.63 39.12
0.80 0.80 2.40 2.40 2.40 0.80 0.00 1.60 3.20 0.00 0.00
14.63 16.42 53.75 57.59 61.16 21.59 0.00 48.81 105.00 0.00 0.00
September (15°C) 6.0 2.56 2.77 6.5 3.01 3.53 7.0 3.45 4.27 7.5 3.89 5.01 8.0 4.35 5.75 8.5 4.78 6.48 9.0 5.22 7.22 9.5 5.67 7.96 10.0 6.11 8.70 10.5 6.55 9.44 11.0 7.00 10.18 Total"2805.04 g m~2 month~1
2.30 2.13 1.96 1.79 1.62 1.45 1.28 1.11 0.94 0.76 0.59
23.63 22.48 21.63 21.03 20.68 20.60 20.76 21.16 21.82 22.83 23.99
60.49 67.66 74.62 81.81 89.96 98.47 108.37 119.98 133.32 149.54 167.93
0.00 2.40 2.40 3.20 0.80 2.40 0.80 5.60 5.60 0.80 1.60
0.00 162.40 179.10 261.78 71.97 236.32 86.69 671.87 746.59 119.63 268.69
N.B. Due to missing data, values of duration of active period and shrimp density for January, are an average of those calculated for May and September.
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Fig. 4. The estimated annual sediment turnover by the mud shrimp Callianassa subterranea at the North Sea study site.
3.5. Estimation of bottom boundary roughness From the seabed photographs (area of view"2.75 m2, depth of field"1.64 m) taken on each of the three main sampling occasions, an attempt was made to evaluate bottom boundary roughness (Zo). In January, the seabed was essentially smooth and it was not possible to discern any discrete mounds attributable to Callianassa subterranea (Plate 1). Bottom boundary roughness, therefore, can be calculated simply using a formula after Kamphuis (see Dyer, 1986), Zo"D/15"0.01/15"0.0007 cm (where D"mean diameter of sediment grain size at the site). In May, suspended sediment load near the bed was so high as to obscure any clear image of the bottom, preventing any estimate of Zo for this month. C. subterranea mounds were clearly visible in September (Plate 2), and 10 individual mound measurements on each replicate image for each of the five stations were made and the real mound size calculated using the appropriate calibration term. In September, mounds had a mean height of 5.4 cm (1SD"$0.1) and a mean base width of 11.7 cm (1SD"$0.9). Using the formula Zo"0.5HS/f [Lettau, 1969, applicable for roughness elements larger than individual grains (i.e., a mound), where H"vertical extent (5.4 cm), S"cross-sectional area (31.59 cm2) and f"horizontal area (107.5 cm2)], the bottom boundary roughness (Zo) for September was estimated as 0.79 cm. 3.6. Estimation of lateral sediment transport An estimation of the amount of lateral sediment transport, derived from Callianassa subterranea’s activity at the study site, was calculated by multiplying the values for expelled sediment rate, transport velocity and particle settling time. Transport velocity is defined as a depth-averaged velocity over the height of ejected sediment, derived
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from estimates of the bottom current speed, shear velocity and boundary roughness length, incorporated into the von Karman—Prandtl equation (see Roberts et al., 1981). Mean near-bed current velocity at the site (Williams et al., 1998), was 5 cm s~1 for both January and September (no corresponding data are available for May), whilst shear velocities were calculated to be 0.17 and 0.52 cm s~1, respectively. The resultant average transport velocities through the sediment ejection plume were estimated to be 3.0 and 2.2 cm s~1, respectively. Particle settling velocity was calculated from Stokes Law, substituting estimates of the density of ejected sediment"1.16g cm~3, mean particle diameter"0.01 cm, density of seawater"1.025 g cm~3, acceleration due to gravity"980 cm s~1, viscosity of seawater"0.0122 g cm~1 s~1 to give a value of 0.06 cm s~1 for all occasions at the site. Particle settling time was then established with knowledge of the height to which sediment was variously ejected (using the laboratory observation that on average the sediment ejection plume height was 3 cm). In January, when there were no mounds present, particles from the middle of an ejection plume would only have to fall 1.5 cm, giving them a settling time of 25 s. Whilst in September, at the other extreme, sediment would be ejected to an average mid-height of 6.9 cm and take 115 s to reach the substratum surface. Combination of the velocity and settling components, with the previously calculated sediment expulsion rates, results in lateral transport estimates of 0.045 kg (dry weight) m~1 month~1 for January and 7 kg (dry weight) m~1 month~1 for September.
4. Discussion In the North Sea, Callianassa subterranea constructs a complex burrow consisting of several vertical shafts which descend from the surface to connect to a maze of horizontal galleries at depths of up to 25 cm (Witbaard and Duineveld, 1989; Rowden and Jones, 1995). Faeces and unwanted sediment, produced by the deposit feeding and burrow maintenance activities of the shrimp, are expelled via a thin exhalant shaft to form a volcano-like mound on the seafloor. The obvious and extensive influence of callianassids upon the substratum in which they burrow suggests that mud shrimps have a significant role in modifying their environment. For example, alterations to the structural and geotechnical characteristics of the substratum have been reported previously for callianassid shrimps (Shinn, 1968; Bird, 1982). Similarly, the findings of companion studies to the present study, show that elevations in the sediment profiles of water and organic content, plus the silt/clay fraction at depth, showed a correlation with the location of the shrimp’s burrow tunnels (Rowden et al., 1998; Rowden and Jones, 1995). Estimates of sediment turnover (or reworking) for members of the Callianassidea, mostly from low latitudes, testify to the prodigious amount of material transported by these shrimps (Aller and Dodge, 1974; Suchanek, 1983). There are few comparable data from temperate regions, but even those demonstrate callianassids’ capacity for moving measurable quantities of material to the sediment surface (MacGinitie, 1934; Ott et al., 1976). Only Witbaard and Duineveld (1989) have published previously an
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Plate 1. Photograph of the seabed at the study site in January 1989, illustrating an essentially smooth bottom.
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Plate 2. Photograph of the seabed at the study site in September 1989, illustrating mounds produced by the mud shrimp Callianassa subterranea.
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estimate of sediment turnover for Callianassa subterranea from essentially the same location as the present study. Their estimate of 3.5 kg (dry weight) m~2 yr~1 is considerably less than the value determined here [11 kg (dry weight) m~2 yr~1]. A possible reason for this discrepancy lies in the methods by which the two estimates were derived. The value arrived at by Witbaard and Duineveld (1989) was extrapolated from a single week’s entrapment of sediment expelled by four individuals (for further difficulties associated with making comparisons see Rowden and Jones, 1993). Our value was based on information of the periodicity of the shrimp’s expulsion behaviour, together with the relationship between body size, temperature and the quantity of sediment expelled. This combination of experimental and field data has allowed the construction of an annual sediment turnover budget for C. subterranea with more rigour than previous estimates for this and other species of callianassid. However, it should be noted that even the present estimate is open to a deal of error (e.g. constructing an annual budget based on three isolated monthly determinations is perhaps questionable) and there is room for improving confidence in particular components of the calculation. None the less, the turnover estimate derived for the population of Callianassa subterranea at the study site in the North Sea indicates that this species of mud shrimp is responsible for transporting a considerable amount of sediment from depth to the surface. Such activity has been shown (for other species of mud shrimp) to have a significant influence upon a variety of physical, chemical and biological processes (Colin et al., 1986; Branch and Pringle, 1987; de Vaugelas and Buscail, 1990). For C. subterranea to date, there is little quantitative evidence documenting the importance, or extent, of its bioturbatory activities [only Swift and Kershaw, 1986 have isolated its role in the redistribution of radionuclides in the Irish Sea]. The aim of the present study was to evaluate the significance of C. subterranea in the process of sediment resuspension, through a combination of its indirect and direct influences. It is widely accepted that expulsion mounds, produced by certain members of the benthos, have the capacity (via the alteration of bed properties) to enhance sediment surface mobility and aid erosional processes (Cadee, 1976; Anderson and Mclusky, 1981). The effective influence of a species in altering bed topography is best evaluated by a change in the measure of bottom boundary roughness, Zo (Nowell et al., 1981). At the North Sea study site, values of Zo increased from 0.0007 cm in January, when the shrimps were relatively inactive, to 0.79 cm in September, when shrimp expulsion activity was apparently at its peak. Values of Zo of 0.00025 cm in January and 1 cm in September deduced by Howarth (1998) from measured depth/current profiles agree closely with the bottom boundary roughness values calculated from the photographs. These data illustrate that, for a portion of the year at least, the mounds of C. subterranea exert a significant influence upon the topography of the seabed and its potential for mobilisation. Nevertheless, increases in Zo due to the activities of C. subterranea were not sufficient to cause entrainment of bed sediment by tidal currents at the study site (Jones et al., 1998). However, the effect may be significant when bed stress is boosted by wave/current interaction (e.g. storms in summer). In addition to an indirect contribution to sediment resuspension, the shrimps’ ejecta have the capacity to go into direct suspension, and to be laterally advected and
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redeposited by near-bed currents. For example, Roberts et al. (1981) demonstrated that the expulsion activity of a Callianassid shrimp made a significant contribution to sediment transport in a Caribbean lagoon. Our present estimate of lateral sediment transport for the site in September [7 kg (dry weight) m~1 month~1] is comparable to the Carribbean value of 8 kg (dry weight) m~1 month~1 (reported as 0.27 kg m~1 day~1). This rate testifies to the potential influence of Callianassa subterranea upon the resuspension of sediment in the North Sea. However, such a capacity varies temporally at the North Sea study site, where a much smaller contribution to lateral sediment transport was estimated for January. Also, at times of increased near-bed currents velocities (storms, peak tides), it is likely that quantities of sediment even greater than those calculated for the month of September would be suspended (evidenced by the obscuration of the seabed in May’s bottom photographs). C. subterranea is thus thought to be the most effective agent of resuspension of bed sediment at this site, as tidal currents resuspended little, except cells/fluff during blooms (Jones et al., 1998). The influence of mud shrimps on the resuspension of sediment in the North Sea as a whole is difficult to estimate because of variabilities related to current strength, temperature, population density and differences in bottom sediment characteristics. Callianassa subterranea, however, has the potential to contribute significantly to the process of sediment resuspension considering its wide geographical range (Kunitzer et al., 1992). Certainly, at our study site where densities were relatively high, it makes a measurable impact upon sediment structure, surface topography and potential for resuspension. Therefore, the activities of C. subterranea must be included in any discussion of the fate of contaminants and the modeling of water quality in the North Sea. Acknowledgements The authors wish to thank the Captain, officers, crew and scientific personnel of the R.R.S. Challenger for their skill and indulgence during all of the named cruises. Thanks are especially due to all those who participated in the arduous and messy ‘Great Shrimp Hunt’. To J. Humphery for the taking of the excellent bottom photographs and his meticulous calculation of the calibration terms. Appreciation is extended to A. McEvoy, S. Widdicombe and J. Latus for variously maintaining the experimental set-up during absences from the laboratory. Finally, amongst many, A. Miller and E. Hickson for useful and enlightening discussions. This work was funded in part by DOE Contract No. PECD 7/8/141. References Aller, R.C., 1978. The effects of animal-sediment interactions on geotechnical processes near the sediment— water interface. In: Wiley, M.L. (Ed.), Estuarine Interactions. Academic Press, New York, pp. 157—172. Aller, R.C., Dodge, R.E., 1974. Animal-sediment relations in a tropical lagoon Discovery Bay, Jamaica. Journal of Marine Research 32, 209—232.
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Anderson, F.E., Mclusky, D.S., 1981. Physical recovery of an intertidal area disturbed by baitworm harvesting. Final report to Natural Environment Research Council Ref. GR3/4061. United Kingdom, 47pp. Bird, E.W., 1982. Population dynamics of the thalassinidean shrimps and their community effects through sediment modification. Ph.D. Thesis, University of Maryland, 42pp. Branch, G.M., Pringle, A., 1987. The impact of the sand prawn Callianassa kraussi (Stebbing) on sediment turnover and on bacteria, meiofauna, and benthic microfauna. Journal of Experimental Marine Biology and Ecology 107, 219—235. Brenchley, G.A., 1981. Disturbance and community structure: an experimental study of bioturbation in marine soft-bottom environments. Journal of Marine Research 39 (4), 767—790. Cadee, G.C., 1976. Sediment reworking by Arenicola marina on tidal flats in the Dutch Wadden Sea. Netherlands Journal for Sea Research 10 (4), 440—460. Christiansen, M.E., Greve, L., 1982. First record of the Thalassinid Callianassa subterranea (Montagu) (CRUSTACEA, DECAPODA) from the coast of Norway. Sarsia 67(3), 213—214. Colin, P.L., Suchanek, T.H., McMurty, G., 1986. Water pumping and particulate resuspension by Callianassids (Crustacea: Thalassinidae) at Enewetak and Bikini Atolls, Marshall Islands. Bulletin of Marine Science 38, 19—24. Dyer, K.R., 1986. Coastal and Estuarine Sediment Dynamics. Wiley, Chichester, pp. 342. Howarth, M.J., 1998. The effect of stratification on tidal current profiles. Continental Shelf Research 18, 1235—1254. Jones, S.E., Jago, C.F., Bale, A.J., Chapman, D., Howland, R.J.M., Jackson, J.J., 1998. Aggregation and resuspension of suspended particulate matter at a seasonally stratified site in the southern North Sea: physical and biological controls.. Continental Shelf Research 18, 1283—1309. Kunitzer, A., Basford, D., Craeymeersch, J.A., Dewarumez, J.M., Dorjes, J., Duineveld, G.C.A., Eleftheriou, A., Heip, C., Herman, P., Kingston, P., Niermann, U., Rachor, E., Rumohr, H., DeWilde. P.A.J., 1992. The benthic infauna of the North Sea: species distribution and assemblages. ICES Journal of Marine Science 49 (2), 127—143. Lee, H., Swartz, R.C., 1980. Biological processes affecting the distribution of pollutants in marine sediments. Part II. Biodeposition and bioturbation. In: Baker, R.A. (Ed.), Contaminants and Sediments, vol 2, Ann Arbor Science Publish. Inc. Ann Arbor, pp. 555—606. Lettau, H., 1969. Note on aerodynamic roughness parameter estimation on the basis of roughness-element description. Journal of Applied Meteorology 8, 828—832. MacGinitie, G.E., 1934. The natural history of Callianassa californiensis (Dana). American Midland Naturalist 15 (2), 166—177. de Man, J.G., 1928. A contribution to the knowledge of twenty two species and three varieties of the Genus Callianassa Leach. Capita Zoology 2 (2), 1—56. Montagu, G., 1808. Description of several marine animals found on the south coast of Devonshire. Transactions of the Linnean Society of London (Zoology) 9, 81—114. Morris. A.W., Howarth, M.J., 1998. Bed stress induced sediment resuspension (SERE 88/89). Continental Shelf Research 18, 1203—1213. Myers, A.C., 1977. Sediment processing in a marine subtidal sandy bottom community: I Physical aspects. Journal of Marine Research 35, 609—632. Nowell, A.R.M., Jumars, P.A., Eckman, J.E., 1981. Effects of biological activity on the entrainment of marine sediments. Marine Geology 42, 133—153. Oyy, J.A., Fuchs, B., Fuchs, R., Malasek, A., 1976. Observations on the biology of Callianassa stebbingi BORRODAILLE and ºpogebia litoralis RISSO and their effect upon the sediment. Senckenberiana Marit 8, 61—79. Posey, M.H., 1986. Changes in a benthic community associated with dense beds of a burrowing deposit feeder Callianassa Californiensis. Marine Ecology Progress Series 31, 15—22. Rhoads, D.C., 1974. Organism-sediment relations on the muddy sea floor. Oceanography and Marine Biology Annual Review 12, 263—300. Rhoads, D.C., Boyer, L.F., 1982. The effects of marine benthos on physical properties of sediments; a successional perspective. In: McCall, P.L., Tevesz, M.J.S. (Eds.), Animal-Sediment Relations; the Biogenic Alteration of Sediments. editors, Plenum Publishing Corporation, New York, pp. 3—52.
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Richards, A.F., Parks, J.M., 1976. Marine Geotechnology: Average sediment properties, selected literature and review of consolidation, stability, and bioturbation — geotechnical interactions in the benthic boundary layer. In: McCave, I.N. (Ed.) The Benthic Boundary Layer, Plenum Press, New York and London, pp, 157—181. Roberts, H.H., Wiseman, W.J., Suchanek, T.H., 1981. Lagoon sediment transport: The significant effect of Callianassa bioturbation. Proceedings of the Fourth International Coral Reef Symposium, Vol. 1 Manila, pp. 459—465. Rowden, A.A., 1993. The burrowing mud shrimp Callianassa subterranea (Decapoda) and bioturbation in the North Sea. Ph. D. Thesis, University of Plymouth, 166pp. Rowden, A.A., Jones, M.B., 1993. Critical evaluation of sediment turnover estimates for Callianassidae (Decapoda: Thalassinidea). Journal of Experimental Marine Biology and Ecology 173, 265—272. Rowden, A.A., Jones, M.B., 1994. A contribution to the biology of the burrowing mud shrimp, Callianassa subterranea (Decapoda: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom 74, 623—635. Rowden, A.A., Jones, M.B., 1995. The burrow structure of the mud shrimp Callianassa subterranea (Decapoda: Thalassinidea) from the North Sea. Journal of Natural History 29, 1155—1165. Rowden, A.A., Jago, C.F., Jones, S.E., 1998. Influence of benthic macrofauna on the geotechnical and geophysical properties of surficial sediment, North Sea. Continental Shelf Research, This Volume. Shinn, E.A., 1968. Burrowing in recent lime sediments of Florida and the Bahamas. Journal of Paleontology 42 (4), 879—894. Suchanek, T.H., 1983. Control of seagrass communities and sediment distribution by Callianassa (Crustacea, Thalassinidea) bioturbation. Journal of Marine Research 41, 281—298. Swift, D.J., Kershaw, P.J., 1986. Bioturbation of contaminated sediments in the north-east Irish Sea. ICES paper, CM 1986/E:18. de Vaugelas, J., Buscail, R., 1990. Organic matter distribution in burrows of the thalassinid crustacean Callichirus laurae, Gulf of Aqaba (Red Sea). Hydrobiologia 207, 269—277. Williams, J.J., Humphery, J.D., Hardcastle, P.D., Wilson, D.J., 1998. Field observations of hydrodynamic conditions and suspended particulate matter in the southern North Sea. Continental Shelf Research 18, 1215—1233. Witbaard, R., Duineveld, G.C.A., 1989. Some aspects of the biology and ecology of the burrowing shrimp Callianassa subterranea (Montagu) (Thalassinidea) from the southern North Sea. Sarsia 74, 209—219.
The role of Callianassa subterranea (Montagu) (THALASSINIDEA) in sediment resuspension in the North Sea A.A. Rowdena,b,*, M.B. Jonesa, A.W. Morrisb a
Department of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK b Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, UK
Received 8 October 1992; received in revised form 17 November 1994; accepted 13 March 1998
Abstract The mud shrimp Callianassa subterranea (Montagu) is a common member of the macrobenthic community at the site in the North Sea selected to study the dynamics of suspended sediment behaviour. The extensive burrowing habit of this deposit-feeding species makes it an important contributor to the degree of bioturbation experienced at the site. Individuals recovered from the site were returned to the laboratory to investigate the influence of body size and temperature upon the amount of sediment expelled. A clear relationship between these variables and the quantity of expelled sediment was identified, and a well-defined temporal pattern of expulsion activity and inactivity was demonstrated. These experimental data, together with field information on seawater temperatures and aspects of mud shrimp population dynamics, allow the construction of an estimated annual sediment turnover budget of 11 kg (dry weight) m~2 yr~1. Field observations at the North Sea site show that the sediment expelled by the mud shrimp forms unconsolidated volcano-like mounds, which significantly modify seabed surface topography. The dimensions of these surface features were measured from bottom photographs of the site and used to determine values of boundary roughness length (Zo). In January Zo was 0.0007 cm, whilst in September Zo equaled 0.79 cm. Callianassa subterranea’s maximum contribution to resuspension was assessed by calculating a derived lateral sediment transport rate of 7 kg m~1 month~1 (from values of near-bed current velocity, modified boundary roughness length and sediment turnover rate). ( 1998 Elsevier Science Ltd. All rights reserved
* Corresponding author. 0278—4343/98/$ — See front matter ( 1998 Elsevier Science Ltd. All rights reserved PII: S 02 7 8— 4 34 3 ( 98 ) 0 00 4 8— X
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1. Introduction The diverse activities of marine benthic organisms resulting in sediment turnover (or reworking) have been a focus of study since the importance of animal—sediment relationships was reviewed by Rhoads (1974). Such bioturbation may alter the geotechnical properties of sediment (Richards and Parks, 1976; Rhoads and Boyer, 1982), affect physical and chemical processes at the sediment—water interface (Aller, 1978), and influence faunal community structure (Myers, 1977; Brenchley, 1981; Posey, 1986). Most major phyla have representatives capable of processing and transporting large quantities of sediment via activities such as feeding and burrowing in both subtidal and intertidal habitats; however, thalassinid crustaceans appear to be dominant sediment reworkers wherever they exist in moderate abundance (for review see Lee and Swartz, 1980). The thalassinid shrimp Callianassa subterranea (Montagu, 1808) is a burrowing deposit feeder, with a wide distribution around the coastal waters of northern Europe from the Mediterranean Sea to the coast of Norway (de Man, 1928; Christiansen and Greve, 1982). In the North Sea, C. subterranea is restricted to water depths of between 30—50 m, where it occurs in muddy-fine sand in densities ranging between 2 and 60 individuals m~2 with a mean of 22 m~2 (Kunitzer et al., 1992). The aims of the current investigation were to quantify the sediment turnover rates for this important bioturbatory species and to evaluate the significance of such activity for sediment resuspension. The work formed part of an interdisciplinary study within the U.K.’s Natural Environment Research Council’s North Sea Project (1987—1992), and developed from a companion study which aimed to identify the influence of benthic macrofauna on the geotechnical and geophysical properties of surficial sediment (Rowden et al., 1998).
2. Materials and methods 2.1. The study site For location and physical characteristics of study site, see Morris and Howarth (1998). 2.2. Shipboard sampling and laboratory sample treatment Macrofauna and sediment — see Materials and Methods section of Rowden et al. (1998). Population structure of Callianassa subterranea — see Materials and Methods section of Rowden and Jones (1994). Seabed photography — In January, May and September 1989, a seabed photographic survey of the site was completed using a ‘cage-type’ UMEL underwater camera assembly. The instrument was deployed 5 times at each station and ‘fired’ automatically 23 cm above the seabed by a contact weight trigger. The survey was conducted at times of lowest tidal current speed to ensure maximum
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potential imaging. Calibration trials with the camera assembly, arranged as per field deployment, allowed the total area and depth of field of view to be calculated, plus the relationship between an object’s imaged and real height/width. Measurements on the negatives were made with the aid of sliding calipers ($0.1 mm) and a stereoscopic microscope (]20). 2.3. Sediment turnover estimates for callianassa subterranea Collection and maintenance — Experimental animals and sediment were collected in April and July 1990 from the station at the centre of the one square sea mile study site. Ten box cores were taken to ensure sufficient animals and sediment to stock laboratory microcosms. Shrimps were hand sorted, placed individually into 1 l pots containing native sediment and seawater, and housed in a constant temperature room adjusted to ambient seawater temperature for the duration of the cruise (2 weeks). Seawater was replaced at 48 hourly intervals. Sediment was frozen aboard the ship to achieve defaunation. During transport to Plymouth (8 h journey), the animals were packed in an insulated container with quantities of ice, whereas the native sediment was uninsulated and refrozen on arrival for storage. 2.3.1. Laboratory design Callianassa subterranea of known sex and size (6.0—10.5 mm carapace length) were placed individually into microcosms made from grey-plastic tubing with wooden bases. Each microcosm measured 30 cm (diameter) by 40 cm (depth) and approximated the natural space requirements of individual animals at the study site (site mean"19 adult shrimps m~2"0.05 m2 individual~1, microcosm surface area "0.07 m2; for population details see Rowden and Jones, 1994). The microcosms, containing native sediment which had been allowed to ‘settle’ for two weeks prior to the introduction of the animals, were arranged within a large tank (approx. 3 m]1 m) of circulating seawater at the temperature encountered at the collection site. The experiment was conducted on three separate occasions using fresh animals acclimatised to the temperatures experienced at the study site in January (7°C), May (9°C) and September (15°C), 1989. 2.3.2. Sample collection and treatment Almost immediately after introduction to the sediment, each animal began to burrow, and records of the burrowing behaviour and surface features produced by the animals were taken at daily intervals. The day after disappearance beneath the sediment surface (deemed day 1), all pseudofaecal and faecal material expelled to the surface was collected (daily for the first seven days, twice weekly thereafter for the experiments at 9 and 15°C, and monthly for those at 7°C). When the exhalant opening of the burrow became conspicuous, a collector (130 ml dessert pot with a hole in its base) was placed over the exit. Expelled material was easily and accurately removed with the aid of a large syringe (60 ml). The collected material was decanted into
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separate pots (250 ml), vacuum filtered (Whatman GF/C 9 mm), washed to remove salt, dried (100°C overnight) and weighed (Sartorius R200D balance -$0.01 g). Opportunistic observations (n"20) were made of the height to which sediment was ejected by the shrimps. The height of the ejection plume was measured by reference to the wall of the collector.
3. Results 3.1. Site characteristics For details of the site’s faunal and sediment geotechnical/geophysical characteristics see Rowden et al. (1998). 3.2. Callianassa subterranea population structure, distribution and density No Callianassa subterranea were recovered in January 1989. This ‘absence’ may be an artefact, as the relatively shallow sampling carried out at that time would not have reached their burrowing depth in colder months (Witbaard and Duineveld, 1989). A restricted quantitative study was undertaken in May 1989 (only sub-cores were sieved), so no suitable data are available for this month. Analysis of C. subterranea numbers in the five box cores taken at the study site for each of the following five visits, showed that individuals were contagiously (patchily) distributed (i.e. the variance is significantly greater than the mean) amongst the samples for October, April and August. In September and July, the distribution was not significantly different from random. Clearly, more samples are required to establish conclusively the within-site distribution of C. subterranea; however, variation in mean density between months was small (38—59 m~2), implying that the population was relatively stable over time, with a mean site density of 46 m~2 (1SD"$8) (for more detail see Rowden and Jones, 1994) 3.3. Sediment turnover estimates for callianassa subterranea 3.3.1. Pattern of sediment expulsion The expulsion activity experiment was designed to calculate the total amount of material expelled to the sediment surface by the Callianassa subterranea population at the North Sea study site via extrapolation of the measured expulsion rates of individuals of known size and sex. The initial construction of the burrow entailed the highest expulsion rates (omitted from subsequent analysis), after which the animal maintained its burrow structure by the ejection of unwanted material during regular and discrete periods of expulsion activity (Fig. 1). These active periods can be most easily characterised by the nature of the time which separates them — deemed ‘inactive periods’ or ‘periods of inactivity’. The periodicity of these inactive periods was defined by calculating the mean duration and frequency of such events for each test animal [duration was simply identified as the mean number of days of inactivity,
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Fig. 1. Sediment expulsion behaviour of the mud shrimp Callianassa subterranea over time (representative example; male, carapace length of 9.5 mm).
whilst frequency was measured as the average occurrence of inactivity in a calender month]. A significant relationship existed between the size of C. subterranea and both components of the inactive periods for individuals maintained at both 9°C and 15°C (Figs. 2A and B). With increasing body size, the periods of inactivity became longer and less frequent. Very little sediment was ejected by C. subterranea kept at 7°C and the consequent low collection frequency did not allow for any description of expulsion behaviour. 3.3.2. Daily expulsion rates Mean daily expulsion rates were calculated for each individual test animal for the periods when Callianassa subterranea was actively ejecting sediment. The results show that the amount of material expelled to the surface mounds was related significantly to size and temperature (Fig. 3). Smaller animals produced less faeces and pseudofeaces than larger ones, and animals experiencing the summer temperature (15°C) expelled greater quantities than those experiencing both the spring (9°C) and winter temperatures (7°C) (ANCOVA; F-ratio"3.893, df"2, 12, P"(0.05). 3.3.3. Monthly sediment processing calculation The population size structure of Callianassa subterranea at the study site, together with the results of the expulsion activity experiment, allow an estimation of the amount of particulate material expelled to the sediment surface by the burrowing and feeding activities of these animals for each of the three study months (Table 1). Regression-derived values for frequency and duration of inactivity enables calculation of the number of days that a shrimp of a particular size actively expels sediment. For example in September, an individual with a carapace length of 6.5 mm had an inactive
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Fig. 2. The relationships between the size of the mud shrimp Callianassa subterranea and the inactive periods of sediment expulsion behaviour, A. Duration (May, r"0.812 P"0.02; September, r"0.911 P"0.001), B. Frequency (May, r"!0.91 P"0.003; September, r"!0.690 P"0.05).
period of 3.53 days which occurred 2.13 times each month. Hence, the amount of time an animal of this size actively expels sediment in a month may be estimated [e.g. for September, 30—(3.53]2.13)"22.48 days]. The monthly expulsion rate for individuals is calculated by multiplying this value by the daily expulsion rate for an animal of a corresponding size, also regression derived [e.g. for September, 6.5 mm: 22.48]3.01"67.66 g (dry weight) month~1]. This rate, when combined with the measured density of C. subterranea, enables a value for expelled sediment per unit area to be achieved [e.g. for September, 6.5 mm: 67.66]2.4"162.38 g (dry weight) m~2 month~1]. Finally, for the larger shrimps, the results of such calculations are summed to give an estimate of the total amount of material the population was responsible for expelling to the sediment-water interface. This results in values of 2.8 kg
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Fig. 3. The relationships between the size of the mud shrimp Callianassa subterranea and sediment expulsion rate, for three experimental temperatures (January, r"0.976 P"0.008; May, r"0.734 P"0.05; September, r"0.824 P"0.02).
(dry weight) m~2 month~1 for September, 0.4 kg (dry weight) m~2 month~1 for May and 0.06 kg (dry weight) m~2 month~1 for January. [Large C. subterranea (6.0— 11.0 mm carapace length) represent a significant proportion of the population’s weight or biomass (e.g. 94% in September; Rowden, 1993) and are also likely to account for almost all of the sediment expelled to the surface as small animals are not thought to be extensive burrowers (Witbaard and Duineveld, 1989)]. 3.4. Calculation of an estimated annual sediment expulsion budget From a non-linear quadratic regression of the sediment expulsion rates (calculated for each of the three study months) against temperature it is possible to obtain estimates corresponding to temperatures between 6—15°C. Combining these predicted values with the monthly seawater temperatures measured at the site during 1989 (BRITISH OCEANOGRAPHIC DATA CENTRE, 1992) an estimated annual pattern of Callianassa subterranea sediment expulsion is obtained (Fig. 4). The model illustrates that the shrimps expel relatively negligible quantities of sediment during the months of January to April [(0.06 kg (dry weight) m~2 month] before they begin to increase output steadily through the spring and early summer [e.g. July"1.3 kg (dry weight) m~2 month~1]. The maximum expulsion rate is achieved at the end of the summer [September"2.8 (dry weight) m~2 month~1], then activity decreases through the autumn before sediment expulsion returns to more modest rates, corresponding to the lower temperatures experienced at the year’s end [December "0.4 kg (dry weight) m~2 month~1]. The summed monthly estimates predict a total annual sediment expulsion of 11 kg (dry weight) m~2 year~1 for C. subterranea at the study site.
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Table 1 Sediment expulsion determinations for the three study months Shrimp size (carapace length -mm)
Sediment expelled in a day (g day~1)
Duration of inactive periods (days)
Frequency of inactive periods (times)
Duration of active period in a month
Sediment expelled in a month (g month~1)
Site shrimp density (indiv. m~2)
Site sediment turnover rate (g m~2 month~2)
January (7°C) 6.0 0.11 — 6.5 0.12 — 7.0 0.13 — 7.5 0.14 — 8.0 0.15 — 8.5 0.16 — 9.0 0.17 — 9.5 0.18 — 10.0 0.19 — 10.5 0.20 — 11.0 0.21 — Total"61.96 g m~2 month~1
— — — — — — — — — — —
24.94 23.29 21.94 20.84 20.02 19.47 19.17 19.14 19.38 19.93 20.70
2.67 2.75 2.81 2.90 2.98 3.12 3.26 3.46 3.70 4.03 4.39
0.40 0.40 2.40 2.80 1.60 1.60 0.40 3.60 4.40 0.40 0.80
1.07 1.10 6.74 8.11 4.77 4.98 1.30 12.47 16.29 1.61 3.51
May (9°C) 6.0 0.70 1.62 6.5 0.85 2.49 7.0 1.01 3.35 7.5 1.16 4.22 8.0 1.32 5.09 8.5 1.47 5.95 9.0 1.63 6.82 9.5 1.78 7.69 10.0 1.94 8.55 10.5 2.09 9.42 11.0 2.25 10.29 Total "378.95 g m~2 month~1
2.94 2.78 2.61 2.45 2.29 2.13 1.97 1.81 1.64 1.48 1.32
26.24 24.09 22.24 20.65 19.35 18.33 17.59 17.12 16.94 17.03 17.41
18.29 20.52 22.40 24.00 25.48 26.98 28.62 30.51 32.81 35.63 39.12
0.80 0.80 2.40 2.40 2.40 0.80 0.00 1.60 3.20 0.00 0.00
14.63 16.42 53.75 57.59 61.16 21.59 0.00 48.81 105.00 0.00 0.00
September (15°C) 6.0 2.56 2.77 6.5 3.01 3.53 7.0 3.45 4.27 7.5 3.89 5.01 8.0 4.35 5.75 8.5 4.78 6.48 9.0 5.22 7.22 9.5 5.67 7.96 10.0 6.11 8.70 10.5 6.55 9.44 11.0 7.00 10.18 Total"2805.04 g m~2 month~1
2.30 2.13 1.96 1.79 1.62 1.45 1.28 1.11 0.94 0.76 0.59
23.63 22.48 21.63 21.03 20.68 20.60 20.76 21.16 21.82 22.83 23.99
60.49 67.66 74.62 81.81 89.96 98.47 108.37 119.98 133.32 149.54 167.93
0.00 2.40 2.40 3.20 0.80 2.40 0.80 5.60 5.60 0.80 1.60
0.00 162.40 179.10 261.78 71.97 236.32 86.69 671.87 746.59 119.63 268.69
N.B. Due to missing data, values of duration of active period and shrimp density for January, are an average of those calculated for May and September.
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Fig. 4. The estimated annual sediment turnover by the mud shrimp Callianassa subterranea at the North Sea study site.
3.5. Estimation of bottom boundary roughness From the seabed photographs (area of view"2.75 m2, depth of field"1.64 m) taken on each of the three main sampling occasions, an attempt was made to evaluate bottom boundary roughness (Zo). In January, the seabed was essentially smooth and it was not possible to discern any discrete mounds attributable to Callianassa subterranea (Plate 1). Bottom boundary roughness, therefore, can be calculated simply using a formula after Kamphuis (see Dyer, 1986), Zo"D/15"0.01/15"0.0007 cm (where D"mean diameter of sediment grain size at the site). In May, suspended sediment load near the bed was so high as to obscure any clear image of the bottom, preventing any estimate of Zo for this month. C. subterranea mounds were clearly visible in September (Plate 2), and 10 individual mound measurements on each replicate image for each of the five stations were made and the real mound size calculated using the appropriate calibration term. In September, mounds had a mean height of 5.4 cm (1SD"$0.1) and a mean base width of 11.7 cm (1SD"$0.9). Using the formula Zo"0.5HS/f [Lettau, 1969, applicable for roughness elements larger than individual grains (i.e., a mound), where H"vertical extent (5.4 cm), S"cross-sectional area (31.59 cm2) and f"horizontal area (107.5 cm2)], the bottom boundary roughness (Zo) for September was estimated as 0.79 cm. 3.6. Estimation of lateral sediment transport An estimation of the amount of lateral sediment transport, derived from Callianassa subterranea’s activity at the study site, was calculated by multiplying the values for expelled sediment rate, transport velocity and particle settling time. Transport velocity is defined as a depth-averaged velocity over the height of ejected sediment, derived
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from estimates of the bottom current speed, shear velocity and boundary roughness length, incorporated into the von Karman—Prandtl equation (see Roberts et al., 1981). Mean near-bed current velocity at the site (Williams et al., 1998), was 5 cm s~1 for both January and September (no corresponding data are available for May), whilst shear velocities were calculated to be 0.17 and 0.52 cm s~1, respectively. The resultant average transport velocities through the sediment ejection plume were estimated to be 3.0 and 2.2 cm s~1, respectively. Particle settling velocity was calculated from Stokes Law, substituting estimates of the density of ejected sediment"1.16g cm~3, mean particle diameter"0.01 cm, density of seawater"1.025 g cm~3, acceleration due to gravity"980 cm s~1, viscosity of seawater"0.0122 g cm~1 s~1 to give a value of 0.06 cm s~1 for all occasions at the site. Particle settling time was then established with knowledge of the height to which sediment was variously ejected (using the laboratory observation that on average the sediment ejection plume height was 3 cm). In January, when there were no mounds present, particles from the middle of an ejection plume would only have to fall 1.5 cm, giving them a settling time of 25 s. Whilst in September, at the other extreme, sediment would be ejected to an average mid-height of 6.9 cm and take 115 s to reach the substratum surface. Combination of the velocity and settling components, with the previously calculated sediment expulsion rates, results in lateral transport estimates of 0.045 kg (dry weight) m~1 month~1 for January and 7 kg (dry weight) m~1 month~1 for September.
4. Discussion In the North Sea, Callianassa subterranea constructs a complex burrow consisting of several vertical shafts which descend from the surface to connect to a maze of horizontal galleries at depths of up to 25 cm (Witbaard and Duineveld, 1989; Rowden and Jones, 1995). Faeces and unwanted sediment, produced by the deposit feeding and burrow maintenance activities of the shrimp, are expelled via a thin exhalant shaft to form a volcano-like mound on the seafloor. The obvious and extensive influence of callianassids upon the substratum in which they burrow suggests that mud shrimps have a significant role in modifying their environment. For example, alterations to the structural and geotechnical characteristics of the substratum have been reported previously for callianassid shrimps (Shinn, 1968; Bird, 1982). Similarly, the findings of companion studies to the present study, show that elevations in the sediment profiles of water and organic content, plus the silt/clay fraction at depth, showed a correlation with the location of the shrimp’s burrow tunnels (Rowden et al., 1998; Rowden and Jones, 1995). Estimates of sediment turnover (or reworking) for members of the Callianassidea, mostly from low latitudes, testify to the prodigious amount of material transported by these shrimps (Aller and Dodge, 1974; Suchanek, 1983). There are few comparable data from temperate regions, but even those demonstrate callianassids’ capacity for moving measurable quantities of material to the sediment surface (MacGinitie, 1934; Ott et al., 1976). Only Witbaard and Duineveld (1989) have published previously an
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Plate 1. Photograph of the seabed at the study site in January 1989, illustrating an essentially smooth bottom.
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Plate 2. Photograph of the seabed at the study site in September 1989, illustrating mounds produced by the mud shrimp Callianassa subterranea.
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estimate of sediment turnover for Callianassa subterranea from essentially the same location as the present study. Their estimate of 3.5 kg (dry weight) m~2 yr~1 is considerably less than the value determined here [11 kg (dry weight) m~2 yr~1]. A possible reason for this discrepancy lies in the methods by which the two estimates were derived. The value arrived at by Witbaard and Duineveld (1989) was extrapolated from a single week’s entrapment of sediment expelled by four individuals (for further difficulties associated with making comparisons see Rowden and Jones, 1993). Our value was based on information of the periodicity of the shrimp’s expulsion behaviour, together with the relationship between body size, temperature and the quantity of sediment expelled. This combination of experimental and field data has allowed the construction of an annual sediment turnover budget for C. subterranea with more rigour than previous estimates for this and other species of callianassid. However, it should be noted that even the present estimate is open to a deal of error (e.g. constructing an annual budget based on three isolated monthly determinations is perhaps questionable) and there is room for improving confidence in particular components of the calculation. None the less, the turnover estimate derived for the population of Callianassa subterranea at the study site in the North Sea indicates that this species of mud shrimp is responsible for transporting a considerable amount of sediment from depth to the surface. Such activity has been shown (for other species of mud shrimp) to have a significant influence upon a variety of physical, chemical and biological processes (Colin et al., 1986; Branch and Pringle, 1987; de Vaugelas and Buscail, 1990). For C. subterranea to date, there is little quantitative evidence documenting the importance, or extent, of its bioturbatory activities [only Swift and Kershaw, 1986 have isolated its role in the redistribution of radionuclides in the Irish Sea]. The aim of the present study was to evaluate the significance of C. subterranea in the process of sediment resuspension, through a combination of its indirect and direct influences. It is widely accepted that expulsion mounds, produced by certain members of the benthos, have the capacity (via the alteration of bed properties) to enhance sediment surface mobility and aid erosional processes (Cadee, 1976; Anderson and Mclusky, 1981). The effective influence of a species in altering bed topography is best evaluated by a change in the measure of bottom boundary roughness, Zo (Nowell et al., 1981). At the North Sea study site, values of Zo increased from 0.0007 cm in January, when the shrimps were relatively inactive, to 0.79 cm in September, when shrimp expulsion activity was apparently at its peak. Values of Zo of 0.00025 cm in January and 1 cm in September deduced by Howarth (1998) from measured depth/current profiles agree closely with the bottom boundary roughness values calculated from the photographs. These data illustrate that, for a portion of the year at least, the mounds of C. subterranea exert a significant influence upon the topography of the seabed and its potential for mobilisation. Nevertheless, increases in Zo due to the activities of C. subterranea were not sufficient to cause entrainment of bed sediment by tidal currents at the study site (Jones et al., 1998). However, the effect may be significant when bed stress is boosted by wave/current interaction (e.g. storms in summer). In addition to an indirect contribution to sediment resuspension, the shrimps’ ejecta have the capacity to go into direct suspension, and to be laterally advected and
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redeposited by near-bed currents. For example, Roberts et al. (1981) demonstrated that the expulsion activity of a Callianassid shrimp made a significant contribution to sediment transport in a Caribbean lagoon. Our present estimate of lateral sediment transport for the site in September [7 kg (dry weight) m~1 month~1] is comparable to the Carribbean value of 8 kg (dry weight) m~1 month~1 (reported as 0.27 kg m~1 day~1). This rate testifies to the potential influence of Callianassa subterranea upon the resuspension of sediment in the North Sea. However, such a capacity varies temporally at the North Sea study site, where a much smaller contribution to lateral sediment transport was estimated for January. Also, at times of increased near-bed currents velocities (storms, peak tides), it is likely that quantities of sediment even greater than those calculated for the month of September would be suspended (evidenced by the obscuration of the seabed in May’s bottom photographs). C. subterranea is thus thought to be the most effective agent of resuspension of bed sediment at this site, as tidal currents resuspended little, except cells/fluff during blooms (Jones et al., 1998). The influence of mud shrimps on the resuspension of sediment in the North Sea as a whole is difficult to estimate because of variabilities related to current strength, temperature, population density and differences in bottom sediment characteristics. Callianassa subterranea, however, has the potential to contribute significantly to the process of sediment resuspension considering its wide geographical range (Kunitzer et al., 1992). Certainly, at our study site where densities were relatively high, it makes a measurable impact upon sediment structure, surface topography and potential for resuspension. Therefore, the activities of C. subterranea must be included in any discussion of the fate of contaminants and the modeling of water quality in the North Sea. Acknowledgements The authors wish to thank the Captain, officers, crew and scientific personnel of the R.R.S. Challenger for their skill and indulgence during all of the named cruises. Thanks are especially due to all those who participated in the arduous and messy ‘Great Shrimp Hunt’. To J. Humphery for the taking of the excellent bottom photographs and his meticulous calculation of the calibration terms. Appreciation is extended to A. McEvoy, S. Widdicombe and J. Latus for variously maintaining the experimental set-up during absences from the laboratory. Finally, amongst many, A. Miller and E. Hickson for useful and enlightening discussions. This work was funded in part by DOE Contract No. PECD 7/8/141. References Aller, R.C., 1978. The effects of animal-sediment interactions on geotechnical processes near the sediment— water interface. In: Wiley, M.L. (Ed.), Estuarine Interactions. Academic Press, New York, pp. 157—172. Aller, R.C., Dodge, R.E., 1974. Animal-sediment relations in a tropical lagoon Discovery Bay, Jamaica. Journal of Marine Research 32, 209—232.
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Richards, A.F., Parks, J.M., 1976. Marine Geotechnology: Average sediment properties, selected literature and review of consolidation, stability, and bioturbation — geotechnical interactions in the benthic boundary layer. In: McCave, I.N. (Ed.) The Benthic Boundary Layer, Plenum Press, New York and London, pp, 157—181. Roberts, H.H., Wiseman, W.J., Suchanek, T.H., 1981. Lagoon sediment transport: The significant effect of Callianassa bioturbation. Proceedings of the Fourth International Coral Reef Symposium, Vol. 1 Manila, pp. 459—465. Rowden, A.A., 1993. The burrowing mud shrimp Callianassa subterranea (Decapoda) and bioturbation in the North Sea. Ph. D. Thesis, University of Plymouth, 166pp. Rowden, A.A., Jones, M.B., 1993. Critical evaluation of sediment turnover estimates for Callianassidae (Decapoda: Thalassinidea). Journal of Experimental Marine Biology and Ecology 173, 265—272. Rowden, A.A., Jones, M.B., 1994. A contribution to the biology of the burrowing mud shrimp, Callianassa subterranea (Decapoda: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom 74, 623—635. Rowden, A.A., Jones, M.B., 1995. The burrow structure of the mud shrimp Callianassa subterranea (Decapoda: Thalassinidea) from the North Sea. Journal of Natural History 29, 1155—1165. Rowden, A.A., Jago, C.F., Jones, S.E., 1998. Influence of benthic macrofauna on the geotechnical and geophysical properties of surficial sediment, North Sea. Continental Shelf Research, This Volume. Shinn, E.A., 1968. Burrowing in recent lime sediments of Florida and the Bahamas. Journal of Paleontology 42 (4), 879—894. Suchanek, T.H., 1983. Control of seagrass communities and sediment distribution by Callianassa (Crustacea, Thalassinidea) bioturbation. Journal of Marine Research 41, 281—298. Swift, D.J., Kershaw, P.J., 1986. Bioturbation of contaminated sediments in the north-east Irish Sea. ICES paper, CM 1986/E:18. de Vaugelas, J., Buscail, R., 1990. Organic matter distribution in burrows of the thalassinid crustacean Callichirus laurae, Gulf of Aqaba (Red Sea). Hydrobiologia 207, 269—277. Williams, J.J., Humphery, J.D., Hardcastle, P.D., Wilson, D.J., 1998. Field observations of hydrodynamic conditions and suspended particulate matter in the southern North Sea. Continental Shelf Research 18, 1215—1233. Witbaard, R., Duineveld, G.C.A., 1989. Some aspects of the biology and ecology of the burrowing shrimp Callianassa subterranea (Montagu) (Thalassinidea) from the southern North Sea. Sarsia 74, 209—219.